1.2.1 Model Fit

There are several basic types of supporting evidence and confirmation:

The first type of evidence that can support the type of natural selection model we have just described is “model fit,” that is, where the predictions of, for example, an optimality model “fit” or predict the outcome that we find in the real population of organisms. We can have model fit of selective models as well, where, after filling in all the blanks in our natural selection model outline in Box 1.1, we can predict correctly what the model outcome would be. We need an example to help understand this.

Biologists David Reznick, John Endler, and colleagues studied life history traits in guppies (see Figure 1.1). “Life history” traits are simply those traits involving the main stages in life, such as development to maturity, reproduction, and aging (Reference Reznick, Travis, Rose and LauderReznick and Travis 1996; Reference Endler, Hecht, Steere and WallaceEndler 1978).

Figure 1.1 Guppies like those studied by Reference Sinervo, Basolo, Rose and LauderSinervo and Basolo (1996)

They studied the hypothesis that life history traits in the guppies were actually adaptations to stage-specific predation that were caused by predators, in other words, adaptations to the rate at which the predators of guppies killed the guppies. Reznick and his colleagues studied two communities that differed in their predators. One type had cichlids as predators – fish that prey heavily on adult-stage guppies – while the other had Rivulus fish that preyed only lightly on guppies, and when they did, it was mostly on juvenile guppies.

Evolutionary theories concerning predation and trade-offs between early and later reproduction made it possible to make predictions about life histories.

The evolutionists investigated the correlation between guppy life histories and the type of predator communities. The first prediction was that an increase in predation on the adults, like that found with the cichlids, would select for a decrease in the age at sexual maturity.

As we can see from Figure 1.2, the measurements from the guppies caught in the wild revealed differences in guppy life histories that were consistent with the predictions. In other words, there was good “model fit.” Guppies from Rivulus localities, where predation was low, were older at maturity than their counterparts from Cichlid localities, where predation was high, which gave the guppies less chance to mature and breed at older ages. Thus, natural selection, according to the hypothesis, evolved guppies that matured earlier and were able to breed at younger ages in the high-predation environment, just as the model predicted. This is an example of directional selection, as illustrated in Figure 1.3. Simple directional or stabilizing selection usually produces peaks in the distribution curves of a trait, and with directional selection, the population average moves over to a new, more desirable, value. (We will examine a case of stabilizing selection in Section 4). Note that this account assumes that the traits are genetically controlled rather than arising from phenotypic plasticity.

Figure 1.2 Decrease of age at sexual maturity depending on predator (Reference Reznick, Travis, Rose and LauderReznick and Travis 1996, p. 266): Least square means (+1 standard error) for the age and size at maturity and size at first birth in females from high- versus low-predation environments. See caption in Reznick and Travis for more information. Think of the predation rates as going from low to high from left to right on the x-axis. The stippled lines represent the means for the Low (Riv/Macro) versus high (Eleo) predation sites. The solid lines are the corresponding values for the high (Cren) and low (Riv) predation sites. All differences between the high- and low-predation sites were significant. (A) Female age at first birth (days). (B) Female size at first birth (wet weight in mg). (C) Male size at maturity (wet weight in mg). (D) Male age at maturity (days).

Figure 1.3 Selection regimes: stabilizing vs. directional selectionFootnote ⁵

This guppy reproduction case is a good example of the good fit of a selective evolutionary model prediction with the data from animals taken from the wild.

1.2.2 Independent Support for Aspects of the Model

As exciting as it is to have selective model predictions be supported by evidence from the wild, there is another distinct type of evidence that can support selection models that may, in many cases, be even more important.

I call it ‘independent support for aspects of the model.’

For example, any selection model includes the assumption that the trait under selection is “heritable,” or reliably passed from generation to generation. This usually means that the trait under selection has a “genetic basis,” or, more accurately, some representation in the cells, development, or genes of the entities under selection.

In the guppy case, Reznick and his colleagues evaluated the genetic basis of the differences in life history traits by doing a simple experiment: They examined the second generation of the wild guppies, which they had bred and grown up in the laboratory. They found that the traits in question did reappear in this later generation, despite the fact that the guppies were removed from their standard selective environment and grew up in a simple glass tank. Thus, the assumption of heritability, or a genetic basis (a genetic/developmental/cellular basis) for the trait, was independently supported. What this claim of “independent support” means is that regardless of how the predictions of the selection model turned out in the wild, the claim that the trait had a heritable basis was supported with lab evidence independent of that prediction.

We could take several of the features in our natural selection model and check to see whether they had independent observational, theoretical, or experimental evidence to support them. These would all count as “independent evidence for aspects of the model.”

1.2.3 Variety of Evidence

A third distinct type of evidence for selection models is variety of evidence, of which there are two kinds. The Variety of Fit amounts to the claim that predictions or outcomes under different conditions using the model are verified. We can see how this works in the guppy case.

Reznick and colleagues (Reference Reznick, Travis, Rose and LauderReznick and Travis 1996; Reference Endler, Hecht, Steere and WallaceEndler 1978) predicted that the guppies from the high-predation sites would devote a higher percentage of consumed resources to reproduction. The model predictions were confirmed in the first experiment, but then, in addition, the model predictions were confirmed in forty new locations, thus adding many cases amounting to a variety of fit (Reference Reznick, Travis, Rose and LauderReznick and Travis 1996).

1.2.4 Totality of Types of Evidence Together

The selective model explaining the origin or maintenance of any adaptation is thus potentially confirmed or supported in a number of different ways by different kinds of evidence (Box 1.4).

2.11.1 Genic and Cellular Levels

At the genic level, we have cases of meiotic drive, wherein sperm cells possess the means to kill off competing sperm cells in a manner that favors inheritance of their own genes, for example, in the t-allele in the house mouse (Reference Lewontin and DunnLewontin and Dunn 1960). The t-allele causes sterility in the male mice it appears in, and demes or groups in which the t-allele is more common clearly have a disadvantage in reproduction. Still, the t-allele persists in the population because it outcompetes other sperm cells at the genic level within gametic reproduction, even though it is selected against at the two higher levels of selection.

On the cellular level, we have the cooptation of eukaryotic (nucleus-containing) cells by free-living bacterial mitochondria, wherein we understand the previously independently living prokaryotic (non–nucleus-containing) mitochondria have been coopted and absorbed cooperatively and symbiotically into the eukaryotic cell (Margulis [Reference SaganAKA Sagan] 1967)). The new eukaryotic cell reproduces both its own DNA and the DNA of the mitochondria in parallel.

2.11.2 Symbiosis Level

These mitochondria are early cases of holobionts, where two independent sets of organismic genomes are linked together through coadaptation and coevolutionary change. Other examples occur with animals and their gut microbiomes (communities of microbes), such as cows and the bacteria, viruses, and fungi that they depend on to digest the cellulose in their diet; similarly for termites, who require their gut microbiome to digest the wood fibers in their diet. There are adaptations that can emerge at the coadaptive level, such as the pedestals built by dung beetles on which they deposit their eggs. When the eggs hatch, they are surrounded by the dung, which contains the gut microbiome that will allow them to thrive in their environments (Reference Lloyd and WadeLloyd and Wade 2019; Reference Suárez and TriviñoSuárez and Triviño 2020; but see Reference Douglas and WerrenDouglas and Werren 2016).

The building of the pedestals made of dung is a joint adaptation of the mutualistic holobiont itself, serving its shared, joint (epistatic) fitness component, as modeled by Reference Lloyd and WadeLloyd and Wade (2019) and as theorized as a “manifester of adaptation” by Reference Suárez and TriviñoSuárez and Triviño (2020; see Reference LloydLloyd 2017).Footnote ¹⁶ While we model such a holobiont as a sort of community or group, let us now consider a more general group-level approach.

2.11.3 Group Level

Consider a group selection case from Michael Wade and community selection case from Charles Goodnight. In the group selection case we must consider genetic interaction, that is, the fact that individual genes’ selective fitnesses are never considered additively in the system, but always in relation and interaction with the other genes in the system, including genes of other organisms in the same social group or family as the original organism.Footnote ¹⁷

Wade offers two card games to help understand what is going on in group selection like this. Take the card game of War, wherein each player lays down a card at each play, and the highest card wins. The cards are totally independent, and there are no interactions with the other cards in the deck. In poker, however, the value of each card depends very much on what other cards you hold in your hand. “Interactions are the essence of poker … .[it has] many possible winning hands, depending on the combinations of cards, the spatial and temporal order in which hands are played, the abilities of the other players in the game, and the past history of hands played by the ‘population’ of players” (Reference WadeWade 2016, p. 190).

There is much evidence for the effectiveness and power of group selection as defined by Wade and Goodnight, both in the laboratory and in the wild. Group selection can produce group adaptive and behavioral changes that allow the group to thrive in otherwise inhospitable conditions.

While many of those taking a genic approach are unaware of the power of group selection, this does not change the status of the empirical evidence nor the likely efficacy of group selection in producing evolutionary change in populations and species in the wild (see Reference LloydLloyd 2005b)Footnote ¹⁸. One of the most striking examples of the success and power of group selection is in the domestic chicken. Chicken breeders had long selected for even tiny improvements in egg-laying rates of hens under domestication, but had not measurably improved their rates due to conflict among the hens in captivity, and their high mortality rate. Group selection on the hens for hen groups that got along better and were more docile, the “kinder, gentler” hens, improved the egg-laying productivity of the hens by up to 60 percent (Reference Cheng and MuirCheng and Muir 2005), thus demonstrating the adaptive power of group selection regimes.

Sometimes when multiple levels of selection are understood to occur simultaneously, this is referred to as “hierarchical selection.” For the classical modeling of such systems, see Sewall Reference WrightWright (1931), or for its first real-world instantiation, see Lewontin and Dunn’s work on the house mouse with its t-allele (Reference Lewontin and Dunn1960).

2.11.4 Lineage Level

Lineage levels of selection may also be effective in producing evolutionary change, at the very least, under the description of product-of-selection adaptations rather than engineering adaptations (see Section 1). Consider, for example, the rates at which lineages speciate, that is, the rate at which they form and branch off new species. This rate varies among different lineages, and interestingly, it varies with the geographic distribution of the species, that is, how the lineage ranges over the Earth, and how it occupies different sectors or areas of the Earth’s geography.

Reference Lloyd and GouldElisabeth A. Lloyd and Stephen Jay Gould (1993) followed the line of thought that lineages of gastropods might develop higher speciation rates depending on their breeding mechanisms, and may also vary in their long-term species survival rates. Those lineages that reproduced in such a way that the young of the species were sedentary and attached themselves to rocks at the beginning of life, thus limiting their range very sharply, were seen as more likely to speciate. The lineages that reproduced by having the young float freely in the seawater were able to travel far from their place of birth and cover a greater geographical range, and were seen as less likely to speciate. Later, the lineage-level adaptive trait of geographic range of offspring in both gastropods and mollusks was found to be correlated with the long-term species survival rate (Reference Jablonski and HuntJablonski and Hunt 2006; Reference JablonskiJablonski 2008). This accorded well with the Lloyd and Gould theory of species selection, which does not require engineering adaptations at the species level, but finds product-of-selection adaptations nonetheless.

“Does this Trait Have a Function?”Footnote ²⁰

If the trait, after investigation, does not appear to have a correlation with fitness,Footnote ²¹ or does not appear to have evidence of design – hence, does not appear to have a current or past function – we pursue other possible evolutionary explanations, such as whether it might be due to genetic linkage with another trait or a by-product of selection (i.e., indirect selection). Alternatively, it may be present due to developmental or embryological constraints, or phyletic inertia, and so on. Pursuit of such explanations consists of testing them against available evidence and searching for new evidence specific to those factors.

However, the approach dominant among leading animal behaviorists, behavioral ecologists, many human evolutionists, and nearly all evolutionary psychologists (who ask evolutionary questions to analyze psychological traits), is the one described above (section 3.1), called methodological adaptationism. Under this approach, the leading research question is: “What is the function of this trait?” And the research consists of a search for supportive evidence for adaptive hypotheses that can explain the trait’s presence in the population.

Issues about method in behavioral ecology and biology revolve around evolutionary adaptations, one of evolution’s biggest successes.Footnote ²² I take it as given that our living world is filled with such adaptations.

Let us examine a defense of an “adaptationist research program” by one of modern evolutionary theory’s founders, Ernst Mayr, written in reaction to Gould and Lewontin’s “Spandrels” paper. Mayr sets up the problem so that selection is the only positive answer to the evolutionary question. He writes:

Mayr offers the discovery of the lateral line in fish – the complex dark line running along the sides of nearly all fish – as an example of the power of the function question; if we had just let the line remain mysterious, we would never have understood its function as an additional sense-organ in the life of fish.Footnote ²³ Moreover, Mayr defends the adaptationist program as harmless, when applied correctly:

Mayr’s approach to adaptationism is widely adopted among evolutionary psychologists, behavioral biologists, and evolutionary ecologists alike.

Thus, identifying the function of a trait is the primary aim of the adaptationist program, which also aims to identify the formative selective pressures. Note that identifying a trait’s function is not necessarily to identify its selection pressure: commonly, for example, we can have multilevel selection, and there are multiple processes responsible for the trait’s form and function. The trait itself does not tell us how to describe its selection pressure, although the investigating biologist may play favorites about which process to privilege in their explanations.Footnote ²⁴

Note also that a trait having utility now is not the same as having a “function” in the selective sense. For example, a trait could contribute to fitness in the current population without having been formed by selection to do so. Reference Gould and VrbaGould and Elisabeth Vrba (1982) dubbed such traits “exaptations”; these have current utility, or “effects,” but not functions in the selective or engineering sense. Evolutionary psychologists and behavioral biologists don’t often use this former category of evolutionary outcome, even when appropriate (see Section 4.4).

Alternately, a trait could have had a function in the past, and a correlation with fitness then, and be a “past adaptation,” with no evolutionary function now, or even be an evolutionary “mismatch” now. Again, human and behavioral evolutionists rarely assign traits to past adaptation, and usually claim current fitness benefits.

While the adaptationist approach may look biased on its face, since it starts with the assumption that the trait is an adaptation rather than one of the other possible features, this assumption is supposed to be only temporary. If it turns out that the trait does not appear to have a function, then the biologist is supposed to move on to other possibilities. This supposedly benign program has been advocated by many biologists since Mayr.

Thus, the methodological adaptationist approach is seen as the “most helpful way to proceed”: look for selective explanation in every case, which upon failure of the selective explanations might lead you to nonselective explanations, which could then be pursued if that is where evidence led (Reference Godfrey-Smith, Orzack and SoberGodfrey-Smith 2001, p. 342). Adaptations are most often indicated by their “specificity, proficiency, precision, efficiency, economy, complexity of design, reliable production, costliness, etc.” (Reference Andrews, Gangestad and MatthewsAndrews et al. 2002a, p. 503 [from Reference WilliamsWilliams 1966]). Optimality models, discussed in Section 1, can be used to investigate these features.

But it is still an open question whether the method outlined here in practice allows nonadaptive explanations to ever win the day. Remember that this issue of “lip service” was a key concern in Reference Gould and LewontinGould and Lewontin (1979). Do researchers in fact find themselves willing to embrace nonadaptive explanations when the evidence points away from adaptation? Other evolutionary factors are often explanatory, but are they appealed to when necessary under the methodological adaptationist approach?

I use what I call the Logic of Research Questions to help unpack and highlight the differences between the relevant theoretical approaches. The logic of the research questions we ask constrains what classes of answers we can give that are responsive and relevant.

Crucially, research questions carry with them an appropriate, unique class of possible and responsive answers, distinct from other contrasting classes of answers. We need to think very hard about the research questions we ask and the answers they allow, because the questions can lead us to miss what’s really going on, and therefore to scientific failure. While I apply this logic to the adaptationist methodology, it can be applied to any scientific investigation; the logic of research questions is applicable to any scientific field that experiences controversy about methods and inference.

The methodological adaptationist asks, echoing Mayr,

Someone following the evolutionary factors framework asks, on the other hand, quite generally:

We can now see a clear logical contrast between the two distinct frameworks and their corresponding sets of research questions and possible responsive answers.

Note that the first answer following the general question, “What evolutionary factors account for the form and distribution of this trait?”, specifically, “Does this trait have a function?”, is an adaptation answer, which was done to suggest that, pragmatically, in the fields of evolution we’re examining, adaptation also is explored, as a priority, in the evolutionary factors methodology. This does not necessarily follow from the evolutionary factors logic, but it is a priority for those in the named fields of study because of their research interests, which center around functions.

But under the evolutionary factors approach, the key question about adaptation is: “Does this trait have a function?” which is logically very different from the key question asked by the methodological adaptationist. Here, there is no assumption that the trait is an adaptation, in sharp contrast to leading research with the question: “What is the function of this trait?” (A reminder for the reader: we are using Williams’ and Lewontin’s notion of an engineering function, not an etiological function; see Section 1.)

Under both the methodological adaptationist and the evolutionary factors approach, there are standards of evidence for when a claim for that factor is supported. When a claim is made that a feature is an adaptation, certain standards of evidence must be met, such as evidence of fitness contributions or design features. The same goes for evolutionary by-products/bonuses, or phyletic features; evidence must be given, in accordance with the standards discussed in Section 1.

Some of the arguments over adaptationism concern these standards of evidence, and nearly all of the focus has been on them, but I claim that some of the root issues concern the initial research questions.

Which question shall we start with? Is the methodological adaptationist question really harmless? Or is there something more being imported into the analysis with that question? Why not use the evolutionary factors research questions all the time?

3.3.1 The “Onerous Burden of Proof” and Its Disappearance

The methodological adaptationists routinely assume that some trait under consideration is an adaptation. Indeed, the research methods of adaptationism have proven very fruitful.

The burden of proof has always been on the adaptationists to demonstrate that a trait has a function and is an adaptation of one sort or another. G. C. Williams is usually quoted concerning the strong burden of proof required for an adaptive explanation:

But Williams himself applied only an informal probability standard for an adaptation: “whether a presumed function is served with sufficient precision, economy, efficiency, etc., to rule out pure chance … as an adequate explanation (p. 10).”Footnote ²⁶ So Williams himself allowed the “onerous burden” of showing adaptation to be satisfied, in practice, by something much weaker than the “objective criteria” he claimed were importantly needed.

Leading behavioral ecologists Reference Reeve and ShermanHudson Kern Reeve and Paul Sherman (1993) also assume adaptation under a wide variety of circumstances, rejecting a widespread definition of adaptation, articulated by the leading philosopher of biology Elliott Sober, as being too weak. Sober requires, for an adaptation: “A is an adaptation for task T in population P if and only if A became prevalent in P because there was selection for A, where the selective advantage of A was due to the fact that A helped perform task T.”Footnote ²⁷

Reeve and Sherman argue there is a big problem with history-laden definitions of adaptation like Sober’s:

Reeve and Sherman recommend counting more things as adaptations at the current time, using current utility: “An adaptation is a phenotypic variant that results in the highest fitness among a specified set of variants in a given environment” (Reference Reeve and Sherman1993, p. 1). Reeve and Sherman use current fitness to infer evolutionary history, that is, promoting to “infer evolutionary causation based on current utility” (Reference Reeve and Sherman1993, p. 2). They claim their approach “decouples adaptations from the evolutionary mechanisms that generate them” (Reference Reeve and Sherman1993, p. 1). This approach to adaptation is akin to what philosopher Bertrand Russell called the “method of ‘postulating’,” which he said “had all the advantages of theft over honest toil” (Reference RussellRussell 1919, p. 71). Thus, an additional problem with methodological adaptationism in practice is that it is prone to shirking its own “onerous burden of proof,” that is, the standards of evidence that are set out in Section 1. It’s easier to change the definition than it is to come up with the evidence of adaptation, so that is what some adaptationists do!

3.3.2 Mistaking Alternatives as Mutually Exclusive Rather Than Complementary Accounts

The logic of research questions under the evolutionary factors framework is a bit different from the logic described by many animal behaviorists, evolutionary psychologists, and other behavioral biology adaptationists, when they practice their craft of explaining the evolution of interesting organismal traits.

The evolutionary factors researcher sees the alternative evolutionary factors as potentially complementary, rather than seeing them as mutually exclusive to a selective approach. Thus, a given trait can be explained primarily through a selective force, but also through a genetic or developmental constraint on that selection, which narrows the range of selective results. In fact, combining factors is very common among evolutionary biologists, as in Wright’s combination drift and selection models (Reference Wright1931), and in the hierarchical selection models of Reference WadeWade (1978, Reference Wade2016) or Reference Odling-Smee, Laland and FeldmanOdling-Smee and colleagues (2003).

Under the evolutionary factors approach, rather than assuming that a trait is an adaptation, we can start our examination of any trait by asking: “Does this trait have a function?”

Also, the evolutionary factors approach acknowledges the division of scientific labor by saying it can be a good idea for some to start by asking about the function of a trait. Similarly, it would be more useful for a systematist to start by asking whether a trait is ancestral or “derived,” and more useful for a developmental biologist to ask how the trait is developed in the organism.Footnote ²⁸ The question we’re facing in this chapter is: Is it useful for anyone to be a methodological adaptationist rather than following an evolutionary factors approach?

For example, contrast the evolutionary factors approach just described with this dualist methodological recommendation from Andrews et al.:

Andrews and colleagues are making a point here about how to increase confidence in a hypothesis: if A and B are “mutually exclusive” exhaustive components, then increasing your confidence in component A commits you to decreasing your confidence in component B, and vice versa.

But the point is both logically and biologically mistaken, since the evolutionary components in question are not truly logically mutually exclusive: They can both be true at the same time. Although being an adaptation and being an exaptation are not mutually compatible, selection can also occur on a spandrel, making that combination also compatible.Footnote ²⁹ Thus, Andrews et al.’s characterizing the factors as “mutually exclusive” is rarely correct in biology. To assert incompatibility is to misunderstand the selective and various other evolutionary factors. They are not only logically compatible, they are biologically compatible.

Reference MayrMayr (1983) made the same mistake: “Only after all attempts to [find an adaptive explanation] have failed, is [the evolutionary biologist] justified in designating the unexplained residue tentatively as a product of chance,” i.e., “the incidental by-product of stochastic processes” (Reference MayrMayr 1983, p. 326; see Reference MillsteinMillstein 2008). Similarly, Reference Buss, Haselton, Shackelford, Bleske and WakefieldBuss et al. (1998) narrow the alternatives to adaptation down to chance and “incidental byproducts,” omitting all the other alternatives (see Box 3.2). This narrowing creates the appearance of having two mutually exclusive disjuncts, but in fact, accumulating evidence for one does not disconfirm all other evolutionary factors.

Modern evolutionary theory says there are evolutionary models available that use distinct evolutionary causes; any of these may answer the question, “What evolutionary factors account for the form and distribution of this trait?” Under this analysis, the causes are not mutually exclusive; they can often be combined and serve as complementary causes of evolutionary change.

The division of labor response says methodological adaptationists are merely researchers who look for functional explanations for traits, and if they cannot find one for a trait, move on to look for another functional solution for another trait. If that were all they were doing, they would be quite harmless. But that is not an accurate description of methodological adaptationism in practice. As we will also see in Section 4, methodological adaptationism leads to bad logic, bad reasoning about evidence, and inferior biology. It is destructive of good science and good evolutionary biology; it is not just a matter of overemphasis on adaptation in the biological community.Footnote ³⁰

But there are even more serious problems that have arisen from methodological adaptationism. In practice, methodological adaptationists sometimes cannot compare the weight of evidence for various hypotheses, one against the other. Even when consideration of evolutionary hypotheses involving the other evolutionary factors really does happen, what counts as evidence supporting those hypotheses fails to come into view, as we shall see.Footnote ³¹

4.1.1 Bonus/By-product Account of Female Orgasm

I have spent over 35 years researching and analyzing the evolutionary explanations for human female orgasm. In my 2005 book, I analyzed 22 distinct theories – all that I could locate at that time – that offered evolutionary explanations for the existence and prevalence of female orgasm; 21 of them were adaptation accounts. I found that none of these 21 accounts were supported by the available empirical evidence that we had about female orgasm at that time.

Eleven of these adaptation accounts were based on a pair-bond view of female orgasm, while several other adaptive accounts were oriented around a female choice sexual selection view that depended on sperm competition and its concomitants (see Section 4.1.4). All of these adaptation accounts were attempting to account for the persistence of the trait in the human population, not its evolutionary origins per se, which might lie in the deep mammalian past, as postulated by Reference Pavličev and WagnerPavlicev and Wagner (2016). The alternative, nondirectly adaptive account for persistence is called the “by-product” or indirect selection account, and is based on strong stabilizing selection in males but not females, as explained below.

The evidential situation has only gotten worse for the 21 adaptive explanations for the prevalence of female orgasm since my book was published, because in 2013 a study of over 8,000 women was published in which the fitness difference that orgasm made for women was studied: The genetic component of fitness difference that the existence and frequency of orgasm made for women was a flat zero (Reference Zietsch and SanttilaZietsch and Santtila 2013). In other words, having orgasm has no effect on genetic fitness, when measured as number of offspring.Footnote ³² If things in the past were like they are today, orgasm cannot have been an adaptation, since it made no difference to reproductive success, a necessary component for an adaptation. Is there any reason to think that things were different in relation to female orgasm in the past? Were pairs in the past more inclined to produce orgasm for the woman upon intercourse, as many have claimed to me, noting that modern women are “professional and uptight”? That argument would have to be substantiated with evidence, which does not look promising according to the world’s authority on primate sexuality, Alan Reference DixsonDixson (2009, 2012).

I concluded in 2005 that the lone available indirectly selective account (which relies on substantial stabilizing selection in males), the by-product/bonus account, had the most evidential support, a position I still hold. The account was first proposed by anthropologist Donald Symons in 1979. An analysis of Symons’ research shows that he is not a methodological adaptationist in the Mayrian sense, but rather an “adaptationist” following the path of the evolutionary factors framework question, “Does this trait have a function?” (See Reference SymonsSymons 1990.)

Symons’ account of female orgasm is based on the shared development of the embryo, as mentioned in the previous chapter. Males and females share the same embryological form at the beginnings of life – they start off with the same basic body plan, and only if the male embryos receive a jolt of hormones during the eighth week of pregnancy do any sexually distinguishing characteristics appear. In males, orgasms are understood to be stabilizing-selected adaptations, likely as rewards for participation in sexual intercourse, which raises reproductive success. In fact, while this is always assumed, it is supported only indirectly with evolutionary evidence of the kind we expect from adaptive accounts (Reference ZukZuk 2006).

The understanding under the bonus/by-product or indirect-selective account of female orgasm is that the females get the orgasm “for free,” that is, simply as a consequence of sharing the embryological form with the male, who is under stabilizing selection for orgasm. The tissues involved in orgasm for males and females are homologues, shared between males and females, including nerve tissues, erectile tissues, and muscle fibers. This whole embryological pattern, not just the clitoris (and potentially involving the five afferent [incoming] sensory nerve pathways I mention in my 2005 book), is involved in producing orgasm in females, and is produced in them through their embryological connection to the same tissues in males. The idea behind the theory is that the tissues involved in orgasm for males and females are very similar, including nerve tissues, erectile tissues, and muscle fibers. Thus, females get the functioning orgasmic tissues through this embryological connection and are capable of having orgasms under the right conditions of rhythmic stimulation.Footnote ³³ Note that this may be seen as both an account of evolutionary origins of the trait, as well as a selective account of the trait’s maintenance in the population.

The bonus, indirect-selective account may also be complementary to the Ovulatory Initiation Hypothesis of Pavlicev and Wagner, who hypothesize a deep origin of the female orgasm in the induced ovulation mechanisms, finding homologies in some of the hormonal releases of both features (Reference Pavličev and WagnerPavlicev and Wagner 2016, Reference Pavličev, Zupan, Barry, Walters, Milano, Kliman and WagnerPavlicev et al. 2019). I find it difficult to understand what the origins of the male orgasm are supposed to be under this account, but again, it may well be complementary to the by-product account, and they both have the same consequences for female orgasm today: Female orgasm is not adaptive, and it does not have a modern evolutionary function.

In any case, the indirect-selective sort of explanation for female orgasm is both ‘developmental’ and adaptive, as we reviewed in Section 2; female orgasms are seen as evolutionary “by-products” of adaptive evolution in the males of the species, just as male nipples are by-products or indirect-selective results of adaptive evolution in the mammalian females. When I first published my book, this more technical use of “by-product” language provoked such a backlash from feminists who accused me of belittling or dismissing the importance of female orgasm (despite my having researched and written a book for 22 years about it) that I have since changed the name to the “bonus/by-product” or more technically correct “indirect-selective” account, or sometimes, the “fantastic bonus” account.

Let us consider the variety of evidence relevant to this case. Note that we are considering supporting evidence for the by-product/bonus account. One common misperception is that supporting evidence for the by-product view must simultaneously be evidence against an adaptive view of female orgasm; but this is not this case and rests on seeing the by-product view as a null hypothesis, which it is not. We will discuss these matters later on in the section.

At the time that my book was published, we didn’t have any fitness results from women’s orgasm, as we do now, showing the lack of connection between fitness and orgasm. We did, however, know the distribution of women’s orgasm rates with intercourse. Since vaginal intercourse is taken to be the behavior most highly correlated with reproductive success and fertility, orgasm rates with intercourse were taken to be significant. Figure 4.1 shows the distribution of orgasm rates with intercourse over a population of women; you’ll notice that the curve is relatively flat, compared to the curves in the selective models shown in Figure 1.3.

Figure 4.1 Orgasm rates with intercourse taken from Reference Dawood, Kirk, Bailey, Andrews and MartinDawood and colleagues 2005

This comparably ‘flat curve’ is represented by an x-axis of overall orgasmic performance, while the y-axis represents frequency in the population.Footnote ³⁴ It shows that the orgasm rate with intercourse never rises above 20 percent for any segment of the female population, in contrast to the selection curves that you see in Figure 1.3 (in Section 1), where the curves feature large percentages of the population – along the lines of 70–90 percent – on the desired value of the trait. Only about 13 percent of women always have orgasm from intercourse (and about half of that is from “assisted” orgasm, that is, orgasm assisted by hand or vibrator stimulation during intercourse), and roughly a third of women rarely or never have orgasm with intercourse, while 5–10 percent of women never have an orgasm at all from any means. The rest fall between – sometimes do, sometimes don’t have orgasm with intercourse. But, again, as we noted in Section 1 and saw illustrated in Figure 1.3, simple directional or balancing selection, which is supposed in nearly all of the selection stories of female orgasm, usually produces substantial peaks in the distribution curves of a trait, peaks encompassing 70–90+ percent of the population. (There is an exception to this expectation; see Section 4.1.4). The fact that women vary so widely in their orgasmic performance thus provides very suggestive evidence that nearly all of the selection explanations offered so far for female orgasm – no matter what their details are – are likely unsupported or disconfirmed. The most recent selective accounts published since my book (for example, Reference Puts, Dawood and WellingPuts and colleagues, 2012a,Reference Puts, Welling, Burriss and Dawoodb) do not address this issue of the lack of a selective peak.

Consider a further variety of evidence for the by-product/bonus account. Strikingly, females masturbate through direct stimulation of the clitoris – the homologous organ to the penis, from the same sources in the embryo – and not through simulating intercourse, just as we would expect on the by-product account. Similar stimulation to homologous organs yields orgasm for both sexes (Kinsey and colleagues 1953). Note the contrast with what we would expect about masturbation if orgasm were selected to go along with intercourse, as it does on all of the adaptive theories: Women would imitate reproductive sex when they masturbated.

In fact, only 1.5 percent of women do this, according to Reference HiteHite (1976) and confirmed by Reference Kinsey, Pomeroy, Martin and GebhardKinsey et al. (1953). Thus, the fact that women stimulate the homologous organ to the penis when they masturbate is predicted by the by-product/bonus account. The origins and maintenance of female orgasm lie with the male-homologous orgasmic structures and reflex (i.e., the clitoris and surrounding tissues), and not in relation to intercourse. The fact that this prediction of the by-product/indirect-selective account is confirmed is evidence in favor of the account.

These facts about masturbation are precisely why Freud thought it necessary to move the locus of excitement from the clitoris to the vagina for “mature” women, because it didn’t make evolutionary or adaptive “sense.” Freud believed that all women ought to have orgasm from vaginal intercourse. This belief was explicitly derived from his conviction that female orgasm must be an evolutionary adaptation to promote reproduction, like many present-day explanations of the trait.

Freudianism said: Female erotic pleasure is initially centered on the clitoris in infancy and childhood, but with the process of maturation into womanhood, the core of female eroticism must ‘migrate’ to the vagina as the healthy woman’s ‘primary’ erotic center (Reference FreudFreud 1905).

As Freud wrote:

Women who failed to enact this migration – that is, the 90–94 percent of women who “obstinately” remained dependent on the clitoris for orgasm, or who failed to reliably have orgasm from intercourse without additional clitoral stimulation – were ‘infantile,’ ‘immature,’ ‘neurotic,’ ‘frigid,’ or ‘dysfunctional.’ Each of the labels is an assault on women’s well-being itself. It’s very significant that this labeling was not restricted to some medicalized or head-shrunken subset of the population – it was the coin of the realm, in women’s magazines and advice columns, in doctors’ advice, and in marriage manuals.

But rather than follow the other evolutionary explanations in enforcing this abuse, the bonus/by-product indirect-selective account actually explains the low rate of reliable female orgasms with intercourse.

It is also supported by new anatomical studies linking the structure of the genitals with orgasm rate with vaginal intercourse. Behavioral endocrinologist Kim Wallen and I discovered that women with a longer distance between their clitoris and urinary meatus (urinary opening, as a more stable substitute for a measure of vaginal opening, the CUMD, “Clitoral-Urinary-Meatus-Distance”) have many fewer orgasms with intercourse than those women with a shorter distance.Footnote ³⁵ Note again that the occurrence of orgasm is not correlated with fitness measures, so these different distances cannot be interpreted functionally, under the present information. The correlation we discovered seems to be an accident of development, not a product of genes, which is confirmed independently by animal studies (Reference Wallen and LloydWallen and Lloyd 2011; see discussion and Figure 4.2 in Section 4.1.4).

Symons’s general thesis is also supported by the nonhuman primate evidence. For example, female stumptail macaques have been shown to have orgasms by placing electrodes into their uteruses and genitals – which shows that they have the distinctive contractions and other bodily markers characteristic of orgasm.

There is a fascinating thing about these orgasms, though. Many of them occur when one female climbs onto the back of another female and rubs her clitoris against the other one’s back, thus providing the direct, rhythmic stimulation desired for orgasm. A few of these same females also have orgasms while copulating with males, but these rates tend to be quite low (Reference LloydLloyd 2005a). In addition, none of the observations about homosexual orgasms were observed to occur during the monkeys’ fertile periods, thus denying any account based on hormones.

All of this is bad news for evolutionary theorists attempting to tell adaptive stories of female orgasm that tie it to heterosexual copulation or fertility, with which this evidence is incompatible. For example, the adaptive hormone-based account of female sexuality says that orgasm will occur during the estrus period of the animal (i.e., when it is fertile), but this is not what is found here, where the orgasms all occurred outside the fertile period, and cannot therefore be related to fertility. These orgasms, however, that are unrelated to heterosexual copulation and to fertility are completely compatible with Symons’ by-product/bonus account, as they link the clitoral stimulation to penile stimulation of the male. This behavior is not compatible with any of the proffered adaptive accounts of female sexuality (Reference Lloyd and GouldLloyd 1993).

4.1.2 Adaptationist Responses to the Bonus/By-product Account of Female Orgasm

In a Reference Alcock1987 discussion in Natural History of my early work presented by Stephen Jay Gould, on the evolution of female orgasm, Gould discussed a variety of empirical evidence in favor of Symons’s by-product/bonus view. Adaptationist Donald Dewsbury, a distinguished psychologist studying animal reproductive behavior, claimed in response to Gould’s discussion

But Gould is actually representing Symons’ views in his quote, and Symons’ views are based on empirical data presented in his chapter; they are not asserted a priori. Gould’s full quote says: “In all the recent Darwinian literature, I believe that Donald Symons is the only scientist who presented what I consider the proper answer – that female orgasm is not an adaptation at all. (See his book, The Evolution of Human Sexuality (Reference Symons1979)).” (Reference GouldGould 1987a, p. 17).

Gould also says:

But Dewsbury’s perception was, clearly, that no good evidence had entered into the debate, despite Symons’s entire book chapter detailing empirical evidence supporting his theory, and Gould’s appeals to the empirical support that I had amassed, involving 14 studies at that time. But all of that empirical evidence (discussed in Section 4.1.3, “‘Null’ Hypotheses”) was invisible to these researchers. Apparently adaptive hypotheses could be favored or disfavored by the evidence – and they had not been favored in the female orgasm case so far – but a nonadaptive hypothesis like the by-product/bonus account apparently could only be “asserted or denied a priori.”

Similarly, many years later, evolutionary psychologists Andrews and colleagues, in considering Gould’s discussion of the female orgasm, claimed that Gould gave no positive evidence for the trait not being an adaptation, under either the contemporary fitness view of adaptation or under a historical functional account, and simply “proclaimed that the female orgasm is not an adaption but a byproduct.”Footnote ³⁶ Andrews et al. complain about Gould’s methodology that:

Note Andrews and colleagues’ requirements of the evidence for something to be shown to be a by-product/bonus. They complain that Gould did not fulfill their evidential requirements, which did not concern positive evidence for the by-product account, but rather, failure at finding an adaptation.Footnote ³⁷

But actually, the repeated failure of adaptationist accounts does not have any bearing on the positive evidence available supporting the bonus/by-product account (reviewed in Box 4.1), although many adaptationists incorrectly believe that this failure of the adaptationist accounts is the sole evidence supporting that indirect selective explanation.Footnote ⁴¹

As we’ll see later on, because the logic of the methodological adaptationists’ research question demands exclusively a function answer, no bonus/by-product answer can be considered a positive answer to their research question, and thus bears support in its favor.

But what about the other evolutionary factors that are allowed in all evolutionary textbooks? Reference Reeve and ShermanReeve and Sherman (1993) allow that there are “mechanisms of persistence other than natural selection,” and they list them as follows: “a relatively non-adaptive trait may persist because of several processes including prolonged lack of genetic variation, unbreakable genetic correlations with other traits, recurrent immigration, and genetic drift” (Reference Reeve and ShermanReeve and Sherman 1993, p. 19). But it turns out that in practice they take these alternative causes, such as developmental constraints or genetic correlation, to either actually be serving the adaptive functions as well, or to not really be viable as alternative causal explanations to adaptive explanations. From this we can see why the list of answers to the methodological adaptationist research question does not actually include any other answers besides the function ones.

4.1.3 “Null” Hypotheses

Ritual recitation of Gould and Lewontin’s “Spandrels” paper in the adaptationist literature usually includes only the lesson that not everything is an adaptation. But this misses one of the primary points of their paper, which includes the problem of the neglect of developmental constraints, phyletic inertia, and laws of form as evolutionary causes. Attention to the logic of research questions illuminates this problem. How can these other factors ever appear on the methodological adaptationist’s list of real, responsive answers?

I argue that methodological adaptationists are committed to this neglect by the logic of their initial orienting question. Once this first move of committing to the question “What is the function of this trait?” is carried out, which seems so innocent, methodological adaptationism is rationally going to lead to error in some cases. This is because starting our biological inquiry by asking the methodological adaptationists’ function-question involves treating nonadaptive hypotheses as something like statistical nulls.

For example, David Barash says explicitly, in a discussion regarding the by-product/bonus theory of female orgasm, that the possibilities include “the ‘null hypothesis’ that it might not be a direct product of evolution after all” (Reference Barash and Lipton2009, p. 133).Footnote ⁴²

In general usage in science or biology, a “null hypothesis” is usually a negative alternative to a positive correlational hypothesis, often used in Neyman-Pearson statistical analyses, one that binds together two variables or terms in a pattern of relations. The use of the “null” hypothesis by behavioral biologists tends to be much more informal, and not to signify necessarily the application of any formal statistical test at all. The positive hypothesis in this case would be one in which a genetic or phenotypic trait was positively correlated with fitness or some component of fitness, while the null hypothesis would be simply a noncorrelation with fitness, often indicating nonselection. An example will bring this out.

John Alcock is the author of the leading textbook on the evolution of animal behavior, but he writes about Gould, who is following my nonadaptive approach to female orgasm: “These are not the claims of someone who wishes to expand the horizon of evolutionary analyses but instead are designed to marginalize the adaptationist approach.” Alcock is thus equating evolutionary causal analyses with adaptationist analyses exclusively (Reference Alcock1998, p. 332). This neglects the fact that the by-product account of female orgasm by Symons is, in fact, an evolutionary causal analysis in its own right.

In another paper, Sherman simply assumes what needs to be shown:

The adaptationists continue to behave as if there’s no supporting evidence for the by-product view, seeing the view as being essentially negative: They see the by-product view as claiming only that no adaptive account has been found, rather than as a positive causal story of indirect selection and its by-products in its own right. Hence their attitude that adopting the by-product view as a live alternative to an adaptationist account of the trait is tantamount to “giving up” on an evolutionary account altogether.Footnote ⁴³

This, however, is the wrong standard scientifically. It presents the scientific situation as all-or-nothing, the adaptation account or no scientific account at all. The by-product/bonus theory is a causal evolutionary account and has its own kind of evidence in its favor (see Reference Beatty and DupreBeatty 1987 for a parallel point about genetic drift). Analysis of the logic of research questions helps make the source and nature of this confusion quite clear.

Let’s review the questions asked by the methodological adaptationists and the researchers using the evolutionary factors framework and their samples of relevant well-formed answers here.

As can be seen by analysis of the logic of these research questions in Box 4.2, then, those using the methodological adaptationist approach cannot appreciate the accumulated positive evidence (see Box 4.1) for the by-product/bonus approach, because they take it as equivalent to a null hypothesis. The by-product account involves positive stabilizing selection on the males, and embryological evidence supporting the linking of the relevant trait with the females of the selected trait, among other evidence, as listed in Box 4.1. This evidence is in some sense only visible on the evolutionary factors framework, where the weight of evidence is the right approach to use in evaluating the by-product/bonus causal hypothesis and its alternatives.

Two points emerge from the discussion above.

First, characterizing the by-product/bonus alternative as a “null” hypothesis leads to the impossibility of positive evidence for what is, in truth, a causal hypothesis, which needs empirical support or refutation. Thus, the attribution of a “null” is mistaken.

Secondly, both the methodological adaptationist and the evolutionary factors theorist can ask about adaptive traits or functions, but the full meaning of the question will not be revealed until we can see what list of answers are live options and under full consideration. As we have seen, the methodological adaptationists may claim to have the same items on their lists as the evolutionary factors theorists, but when push comes to shove, they do not treat them as live options, on their own accounts.

We can zero in on the key problem: None of this evidence for the causal by-product/bonus hypothesis in Box 4.1 is recognized or weighed when considering this trait from the adaptationist methodological perspective. Thus, even though the methodological adaptationists present their adherence to their research program and its attendant question as perfectly harmless and, in fact, very good and productive science, we can see here an example of where it goes astray. Because they implicitly assume that no null hypothesis may have evidence in its support, they cannot see the evidence supporting the by-product/bonus account.

4.1.4 Critics of the By-product Account and Evidence

The leading critics of the by-product/indirect selection account continue to support adaptive accounts. Let us compare the status of the empirical evidence supporting the most favored current adaptive account (Reference Puts, Dawood and WellingPuts et al. 2012a,Reference Puts, Welling, Burriss and Dawoodb, Box 4.4) with the evidence supporting the bonus/by-product account, as given in Box 4.1. Recall that, according to 37 studies of 148,346 women using 27 metrics in the various studies, only about 20 percent of women reliably have orgasm with intercourse, including with hand-or-vibrator-assisted intercourse, while about 90 percent of the female population does have orgasm sometime during their lives (Reference LloydLloyd 2005a). So, while orgasm is present in the vast majority of women, it does not routinely appear in the ordinary evolutionarily relevant context, that is, vaginal intercourse.

Box 4.4Visualization of Reference Baker and BellisBaker and Bellis 1993 Data Set from Pairs in Study

The by-product/bonus account gives a cogent explanation for this glaring fact. However, we should note that not every evolutionary explanation must produce frequent orgasm with intercourse, under our current theories. Consider a female choice account with sperm “upsuck,” as shown in Box 4.3.

Puts and colleagues’ female choice/upsuck account posits that females mate multiple times over a short period of time with different males. The basic idea is that the female will have orgasm preferentially with the higher-quality males. Orgasm is assumed to be accompanied by a mechanism of uterine upsuck that makes it more likely that the female will be fertilized by the higher-quality male. Thus, the orgasmic women are required to respond with orgasms only sometimes with intercourse – “yes” with high-quality males, and “no” with lower-quality males. The model says this will produce more and/or better offspring. In Box 4.3 there is the sketch of the female choice selection model and its level of evidence. But look at their data (Box 4.4).

Alan Dixson, again, the world authority on comparative primate sexuality, denies that this sort of “cryptic female choice” selection occurs in human beings (Reference Dixson2012, p. 630), in which females have a mechanism to “choose” or prefer the sperm of higher-quality males to fertilize their eggs. Dixson gives a series of reasons why this is not so, including the lack of specialization in the penis, the lack of specific structures in the sperm, the lack of evidence for uterine upsuck,Footnote ⁵⁰ and so on, all of which, in other species of primates, accompany cryptic female choice and sperm competition as hypothesized in the upsuck theory, and its associated hypothesis of female choice.

Under the upsuck theory, female orgasm is accompanied by a sucking motion of the uterus. This “uterine or sperm upsuck” theory is an old piece of folk wisdom dating back to the Ancient Greeks, but it has never enjoyed any real evidential support, although people have been seeking scientific evidence to support it for over 70 years. There is actually evidence against it from a set of nicely designed experiments done by Reference Masters, Johnson and MoneyMasters and Johnson in the 1960s (1965; Reference Masters and Johnson1966)

Nevertheless, the upsuck hypothesis is very widely believed by laypeople, especially due to a deceptive narration of a video clip shown on TV,Footnote ⁵¹ and had achieved widespread acceptance among scientists since the 1990s, through the work of Robin Baker and Mark Bellis published in 1993, which claimed to provide empirical evidence supporting the phenomenon.

In one “supporting” data set, they have 1 out of 11 couples in the sample contributing 93 out of the 127 data points (nearly three-quarters of the data!). Four of the other 10 couples contributed one data point each, a combined total of 3 percent of the data, and so on. But extrapolating to the population at large based primarily on the results of a single subject badly violates standard statistical practice (see Reference LloydLloyd 2005a, Ch. 7). In the end, the Baker and Bellis data are statistically worthless and no scientific conclusions can be drawn from them.

So why was this account of uterine upsuck adopted by top researchers in human evolution and taught in human evolution courses by evolutionary psychologists and sociobiologists? It cannot be because the paper was good science – because it clearly wasn’t – as even my harshest critics now agree (e.g., Reference BarashBarash 2005). It seems to be because they just liked what the paper had to say, namely that female orgasm serves an evolutionary function. Here we see adaptationist bias in action, and several adaptationists, David Puts and Khytam Dawood and colleagues, are still citing this Baker and Bellis paper to underpin their female choice theories (e.g., Reference Puts, Dawood and WellingPuts et al. 2012a, b) despite having given no real defense of the paper against the critique I gave in 2005, among other methodological critiques.

In Box 4.3 is the state of the empirical evidence supporting the various aspects of the female choice/upsuck selection model, accompanied by their sources. As you can see from Box 4.3, the model is not well supported by the empirical evidence.

But if we look just at the prediction of this particular sexual selection model, it can successfully be tweaked to fit the evidence of the flat curve showing orgasm rate with intercourse, as in Box 4.1. The poor state of evidential support for the hypothesis is only made clear by checking the independent evidence for the various aspects of the model, the central and crucial step in evaluating an adaptive hypothesis, as we saw in Section 1. Thus, the only adaptive model that is compatible with the sexology evidence – in that it fits the flat curve – does not have further supporting evidence for its aspects and assumptions. Thus, the female choice model is not comparable to the by-product account in its overall evidential support.

There is further evidence in favor of the by-product account. One of the most compelling things about the female choice theory is that it gives an answer to the question “Why do women respond to intercourse with orgasm sometimes yes, sometimes no?”, which was mysterious under other adaptive theories.

Kim Wallen and I published independently confirmed analyses of data that bear directly on whether or not women have orgasm with intercourse, and when. As mentioned above, our anatomical, non-adaptive, explanation of why women have a variety of orgasm rates is based on what we call “CUMD” measurements, the measured distance between the clitoris and the urinary opening, meant to stand in as a proxy for the vaginal opening.

Figure 4.2 shows some of our data.

Figure 4.2 Wallen and Lloyd CUMD

The white bars represent women who reliably do have orgasm with intercourse, while the black bars represent women who routinely do not have orgasm with intercourse. On the y-axis is the CUMD.

You can see that the women who routinely have orgasm with intercourse have much shorter CUMD measures than the women who do not. The difference between the groups in orgasm rate is highly significant, greater than two standard deviations, in both data groups that we analyzed, Bonapart and Landis. This anatomical trait is apparently due to developmental exposure to androgens in the womb and is not genetically controlled.

Using an independent statistical test, we also found that this anatomical distance was predictive of whether a woman had orgasm with intercourse. You can also see that it was irrelevant to orgasm with masturbation, as we would expect.

In other words, we found that an anatomical trait predicted whether or not a woman would have orgasm with intercourse. This makes good sense, if you think about it. In sum, Wallen and I found that for the strong majority of women in our samples, anatomy seems to suggest destiny (Reference Wallen and Lloyd2011). And clearly, if her anatomy so strongly influences whether or not she has an orgasm with intercourse with a male, that leaves insufficient room for the genetic quality of the male – specifically, his masculinity, attractiveness, or dominance, as presented in the female choice theories – to strongly influence the outcome of such intercourse, with orgasm accompanied by uterine upsuck.

This is because, according to the population genetic theorists, the selection pressure of this type of sexual selection scenario needs to be quite strong in order to produce any result in terms of evolution (Reference HoskenHosken 2008). Thus, the anatomical relation we discovered makes such a scenario highly unfeasible. In other words, there is no evidence that the women’s variation in orgasmic response, as measured in CUMD, coordinates with the masculine features emphasized by the female choice theories. It seems, rather, that women either tend to have orgasm with intercourse or not, depending upon their anatomical features and not their partners. As we move along the flat curve, those women either tend or don’t tend to have orgasm with intercourse, regardless of their male partners. But the prevailing selective theory needs them to be very sensitive to male traits against the available evidence.

Thus, the female choice theory does not have further supporting evidence for its aspects and assumptions, and thus is not comparable to the by-product account in its overall evidential support, as one can see by following up on the evidence cited in the footnotes. We can see this quite clearly when we contrast this sexual selection/cryptic female choice adaptation model (Box 4.3) with the one for the bonus/by-product/indirect selective account (Box 4.5).

Note that in both cases, there is evidence for no function of orgasm in females, which is nonresponsive to the research question of the methodological adaptationists, “What is the function of this trait?” Instead, the by-product/bonus explanation is better seen as an answer to the evolutionary factors research question, “What evolutionary factors account for the form and distribution of this trait?”

This is the correct reading of the bonus/by-product theory of female orgasm, as a positive alternative causal hypothesis, not as a null hypothesis. It is an alternative to the previous, function answers to the methodological adaptationists’ question, and it is an answer that is not on their list of possible answers, which only includes answers like: “The function of female orgasm is to preferentially mate with high-quality males,” or “The function of female orgasm is to aid the pair bond,” and so on.

To illustrate the dangerous and unscientific consequences of methodological adaptationism in this particular case: Several prominent adaptationists repeatedly complain that under the by-product/indirect selection hypothesis, female orgasm would fade away and deteriorate over evolutionary time and would disappear from the population. This mistaken inference has been advanced not only by leading scientists such as Alcock, Sherman, and Barash, but also by feminist primatologist and human evolutionist Sarah Blaffer Hrdy, and it is based on a misunderstanding of both how the by-product/bonus account works, and the evolutionary factors framework itself.Footnote ⁵⁷ These misunderstandings are likely a consequence of their adaptationist bias that a particular trait will only be sustained in a population if it itself is under sustained selective pressure. But under the bonus/by-product account, the basic muscle, nerve, and tissue pathways involved in female orgasm would be maintained in the female over the generations in virtue of the fact that they are under ongoing strong stabilizing selection in the male; male nipples are maintained in the same fashion. Nobody thinks that male nipples are disappearing! Thus, methodological adaptationist explanatory biases involving the necessity of selection have led to fundamental mistakes regarding the by-product/bonus hypothesis by these researchers and their followers.

In addition, when discussing alternatives to adaptations, methodological adaptationists have been prone to make further scientific errors concerning what the by-product/bonus account says and assumes. These biologists reason that if a trait is not adaptive, it cannot be part of an evolutionary account at all.

On John Alcock’s analysis, the by-product/bonus hypothesis is a null result and offers only a “proximate” explanation of how women come to have orgasms.

For Alcock, who calls himself an “ardent adaptationist,” the by-product explanation is seen as no evolutionary explanation at all. On Alcock’s analysis, which is shared by Paul Sherman, a leading theoretician of animal behavior, the by-product hypothesis offers only a “proximate” explanation of how women come to have orgasms. In other words, it only explains how female babies grow up to have orgasms as adult women.

Alcock writes that

Thus, the by-product account is not seen as an evolutionary account at all – it is not an answer to any evolutionary question about female orgasm, with supporting evidence and theoretical standing in evolutionary theory.

Here we can also look to David Barash, the author of the most widely selling textbook on sociobiology for a couple of decades and a grandfather of the field of human evolution, who writes, with his wife, in a sympathetic discussion regarding the impetus behind those favoring the by-product/bonus theory, that it involves

Note the equivalence of evolution with selection in this statement; the bonus/by-product explanation is mistakenly not considered evolutionary, just as we saw before with Alcock and Sherman. This is again the result of the logic of the research question, through methodological adaptationism.

For these authors, unless we are allowed to assume there is an adaptation, then we cannot tell whether we can explain it in an “evolutionary” way. The entire rest of evolutionary biology that we have been discussing in the evolutionary factors methodology is invisible, under this account; it is disappeared. The methodological adaptationists’ methodology was supposed to be benign; it was not supposed to be a risky endeavor with radical theoretical commitments, although that is where it seems to have ended up.

4.1.5 Beyond the Comfortable Boundaries of Adaptation: The Logic of Research Questions

In this section, I have been emphasizing the initial patterns of inference and explanation, of exploration and investigation, rather than the final “evidentiary standards,” that are often emphasized and discussed when considering adaptations. My focus here is much more on the investigative standards, and less on the evidential standards. My point is that if you use the methodological adaptationist research question, the evidentiary standards of alternatives like the by-product/bonus view, accurately portrayed, never come up, since they are buried under the assumptions regarding the null hypothesis and other myths. Gould and Lewontin’s just-so story objection is about the standards of evidence, but I have identified the deeper danger earlier, which is in the logic of the research questions asked, particularly in the consequences of the methodological adaptationist research question and its possible and responsive answers all being “function” answers.

Many adaptationist researchers approaching the evolution of female orgasm start with the methodological adaptationist research question:

“What is the evolutionary function of female orgasm?”

Other evolutionists, though, may ask:

“What evolutionary factors account for the form and distribution of female orgasm?”

My claim is that the possible and responsive answers to these evolutionary questions are relevantly and significantly different. These are questions and answers with consequences.

For instance, an evolutionary account of female orgasm is used to underpin a notion of the normal function of female orgasm for the diagnostic and statistical manual of the psychiatric profession, the DSM V by which sexual disorders are diagnosed.Footnote ⁵⁸ But in evolutionary science, there is no single accepted adaptive account of female orgasm, and thus no notion of its ‘normal function,’ if it has any at all.

The fact that the adaptationists see the by-product view only as a null hypothesis or as a nonanswer to the adaptive question leads directly to their mistaken characterizations and inferences involving the view. I am concerned with what it would take to get a community of adaptationists to move far enough beyond their research orientation and their driving adaptationist question to start approaching things from the broader, evolutionary factors point of view.

What would it take for these researchers to consider seriously the alternatives of the evolutionary factors approach, which are acknowledged to be real contenders for valid evolutionary explanation?

This case of the female orgasm reveals that there is something peculiar and implausible about methodological adaptationism as it’s usually advanced, namely, that the researcher is envisioned as, at some time in the middle of their research program, abandoning their research commitments and explanatory practices, in the face of some facts or others, and then going along some completely different explanatory pathway. This is a lot to ask a researcher to do; they need to do a sort of mental gymnastics, and few – in fact, none – of the methodological adaptationist researchers involved with the evolution of female orgasm have been able or willing to do that.

In sum, this case highlights issues with the evidence needed for adaptive explanations that are pertinent to the study of development and by-products, and how confusing to biologists it sometimes is to move beyond the comfortable boundaries of assuming that a trait is an adaptation.

Let us consider some other cases in which developmental biology and developmental genetics play a significant role in evolutionary explanation and examine how adaptation explanations might work in counterpoint to evolutionary factors ones.

4.4.1 Background

There is one final type of evolutionary factor to consider before we close our consideration of adaptation. In 1982, Stephen Jay Gould and Elisabeth Vrba coined a new term, “exaptation,” to mean a trait that contributes to fitness but was not selected to do so. It was meant to contrast with “adaptation” (see Table 1.1). They also said that any trait that contributes to current fitness is an “aptation,” which encompassed both adaptations and exaptations. The skull sutures in human babies (Figure 2.2) are a perfect example of an exaptation; they contribute to fitness, without having been built by selection for that purpose, that is, they are something with “vital current utility based on a cooptation of structures evolved in other contexts and for other purposes (or perhaps for no purpose at all)” (Reference GouldGould 1991, p. 46). In other words, we have a trait that does not vary within the population, such as the existence of skull sutures in mammals, but which increases fitness over possible (but never actual) alternative traits, such as not having any skull sutures. If there had ever been significant variation in skull sutures, they would be selected against during birth, but there is not, so they are neither engineering nor selection-product adaptations. But they do contribute to fitness in mammals, in easing birth, so they are “aptations,” with no history of selection, since baby skull sutures are just like reptile skull sutures, products of developmental constraint or architecture.

Exaptations became significant in a debate within evolutionary psychology in the early and mid-1990s, primarily because of an intervention by Gould, who claimed that many brain activities were likely to be exaptations – that is, effects that contribute to fitness, but were not selected to do so – rather than genuinely selected evolutionary functions in both the etiological and engineering sense.

This went against the orthodoxy of evolutionary psychology at the time, which was led by methodological adaptationists and was more inclined toward interpreting obviously fitness-increasing brain activities as evolutionarily selected functions.Footnote ⁶⁴

Unfortunately, in the context of that debate, Gould made an error of speaking and used the term “function” in the vernacular, or commonsense, manner, rather than in the technical, evolutionary engineering sense, as we shall see in a moment. Later on, some methodological adaptationists mistakenly took this occasion of Gould’s misspeaking as confirmation that ‘exaptation’ had an evolutionarily ‘designed’ function and was a version of an engineering adaptation. This was a mistake because exaptation is not a version of adaptation; it is a distinct form of aptation. As a result, other methodological adaptationists provided a standard of evidence for exaptation that was inappropriate and based on an adaptationist worldview. These ideas have been rendered practically useless through their mistaken definitions and misapplications by some evolutionary psychologists over these last decades.

4.4.2 Evolutionary Function, a Misspoken Phrase, and a Misunderstanding

Various discussions of Reference Gould and VrbaGould and Vrba’s (1982) concept of ‘exaptation’ have been plagued by terminological ambiguity. Specifically, varying uses of the concepts of ‘current utility’ and ‘function’ have contributed to uncertainty about when and how the notion of ‘exaptation’ should be used (see Table 1.1 for definitions). In this section, I shall focus on the issue of exaptation as it is discussed in two characteristic, widely cited, and very influential papers by Reference Buss, Haselton, Shackelford, Bleske and WakefieldDavid M. Buss, Martie G. Haselton, Todd K. Shackelford, April L. Bleske, and Jerome C. Wakefield (1998)Footnote ⁶⁵, and Reference Andrews, Gangestad and MatthewsPaul W. Andrews, Steven W. Gangestad, and Dan Matthews (2002a)Footnote ⁶⁶.

In a widely cited paper aimed at explaining to psychologists the concepts of ‘adaptation,’ ‘exaptation,’ and ‘spandrels,’ Reference Buss, Haselton, Shackelford, Bleske and WakefieldDavid Buss and colleagues (1998) attempt to delineate the meanings and evidential requirements of these three terms. The notion of ‘function’ plays a central role in their analysis. In discussing adaptations, they write, “to propose that a trait is an adaptation is to propose that it was designed by natural selection in past environments to serve some function” (emphasis added; Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 85). Thus, they are using the same notions of function and adaptation we introduced in Section 1.

Now let us look at the way that Gould and Vrba used the term ‘function’ in their discussions of exaptation. The term ‘exaptation’ applies to two types of traits:

1. 1. Traits that were adapted for one evolutionary function but were later co-opted (but not selected) to serve a different role; and

2. 2. Traits that were correlates of growth, or accidental by-products, or “spandrels,” that were later co-opted (but not selected) to serve another role.

Gould and Vrba also follow George Williams’ terminology regarding function, stating that “the operation of an adaptation is its function,”Footnote ⁶⁷ just as we find in Section 1. Similarly, the operation of a useful character not built by selection for its current evolutionary role is an “effect.” Exaptations’ effects do contribute to current fitness, by definition, but are not designed or selected to do so. “Adaptations have functions; exaptations have effects” (Reference Gould and VrbaGould and Vrba 1982, p. 6; emphasis added).

Gould and Vrba also suggest that the general phenomenon of being fit for a specific evolutionary role (current fitness) should be called ‘aptation’ rather than the usual ‘adaptation’. This allows for a distinction between traits selected for the current role, and those not. The most important part of these definitions is that exaptations must contribute to present fitness, but were not selected, historically, to do so. This is as opposed to adaptations that also contribute to present fitness, but which were naturally selected for their contributions to fitness and evolution of an adaptation in the past.

The regular requirements for adaptations demand that an adaptive account explain the adaptive feature(s) or modification(s) acquired through the selective process over time, its ‘engineering’ history of its complex and built-up adaptive traits. Under these definitions, both adaptations and secondary adaptations have selective histories, but exaptations do not. Recall that this definition of adaptation contrasts to the “product of selection” definition.

Note here that there is an important distinction to be made between secondary adaptations, which can be maintained by directional, stabilizing, or other forces of selection, and exaptations, which are not primarily maintained by selection. Stabilizing selection is therefore not the primary explanation of stability in the trait. Rather, exaptations maintain their status primarily through other biological mechanisms, such as developmental constraints, embryological considerations, or other structural means such as by-products or genetic correlations. The claim is: Selection is not the evolutionary cause that is maintaining the trait where it is.Footnote ⁶⁸

Significantly, exaptations can be modified by selection to serve yet a new evolutionary function: to become “secondary adaptations.” For example, feathers originally served as exaptations for flight, under the assumption that they originally evolved for thermoregulation of the dinosaurs they appeared on. It is hypothesized that they were then utilized for short flights. However, the various subsequent modifications of feathers for flight are secondary adaptations, thus making certain features of the feathers engineering secondary adaptations themselves (Reference Gould and VrbaGould and Vrba 1982, p. 11). Contrary to a common objection, it is not the case that one generation of use in flight makes the feathers an engineering secondary adaptation, which requires generations of genetic change and distribution of that genetic change throughout the populations of the species. Only after such distributed genetic change and the acquisition of such genetic change and adaptive features by members of the species is the feather considered to be an engineering secondary adaptation for flight.

Thus, if there is a stable trait in the population that contributes to fitness, on its face, it might be either an adaptation or an exaptation; it is simply an “aptation.” It might have arrived at its present state through a selection process, in which case it is either a primary or a secondary adaptation. It may also have attained its current identity primarily through embryological or developmental constraints, and other structural features. The point is that these can explain why it is stable in the population, as an alternative and complement to stabilizing selection or other forces of selection. Relevant mechanisms might include genetic constraints and developmental details of the organism, correlations of growth, and by-products of other features of the organism. For example, the constancy of having seven cervical vertebrae in mammals, including mice, humans, and giraffes, has been revealed as a product of the involvement of Hox genes (related to the Bicoid case) and developmental constraints (Reference GalisGalis 1999).

Take the case of a novel use of a trait in a fitness-enhancing way. For example, an insect allele that was neutral before but in a new context provides protection against a novel pesticide would be, in the first exposure, not a selection-product or engineering adaptation for resistance until it undergoes natural selection (i.e., differential reproduction relying on this allele’s protection). After selection, it would be considered a selection-product adaptation, as there is no new machinery or built-up trait involved in the process, but rather simple differential survival of the alleles (Reference Lloyd, Rama, Krimbas, Beatty and PaulLloyd 2001).

When Buss and colleagues confuse evolutionary “function” with exaptation’s effects, they ignore this important point.

4.4.3 The Difference between Function and Effect

In a Reference Gould1991 paper, Gould was not completely careful in separating “function” and “effect,” and his misspeaking has led to a great deal of confusion. The occasion of the confusion was that Gould once described exaptation as “a feature, now useful to an organism, which did not arise as an adaptation for its present role, but was subsequently co-opted for its current function” (Reference Gould1991, p. 43, my emphasis). Here, Gould misspeaks and does not use “function” to refer strictly to the activity of an engineering adaptation. He instead uses “function” in a more vernacular sense so that it misleadingly appears to signify the useful action of a selected trait. Gould makes clear that such action involves enhancing current fitness (Reference Gould1991, p. 47).

This combination of statements led Buss and colleagues, due to their adaptationist biases, to conclude that an exaptation must have a “function” in the stricter, adaptive sense (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 539). Buss and colleagues end up confusing the requirement that exaptations contribute to current fitness with their own, added requirement that they serve a “function,” understood as a solution to an adaptive problem. What is at stake in the confusion is the relative importance of using natural selection versus other evolutionary factors to account for currently useful, ‘aptive,’ fitness-enhancing traits, and in general, the overall power of adaptive explanations.

They contrast selective functions, which for Buss et al. include exaptations, with “biologically functionless uses,” which they refer to as “effects,” “consequences,” or “byproducts” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 539). Thus, they have severely altered Gould and Vrba’s terminology when they exclude “effects” from the performance of exaptations. These effects are precisely what Gould and Vrba defined as the outcomes of exaptations! What Buss and colleagues have described here are, in fact, secondary adaptations, not the original nonadaptations that signify “exaptations.”

4.4.4 Applying the Logic of Research Questions

Let’s look at this using the Logic of Research Questions.

As we can see, Buss and colleagues have mistakenly turned a nonresponsive answer, the true exaptationist position, into a responsive answer that satisfies their function research question (See Box 4.11, below). As such, the actual definition of ‘exaptation’ is missing and is not being actively considered by the evolutionary psychologists under their research question in a paper that has been cited over 900 times.

The alternative, “Evolutionary Factors” research question, offers the full variety of evolutionary explanations, including adaptation through selection, exaptation through cooptation (under the original definition), and so on. These questions and a few of their answers can be seen in Box 4.12.

Under the evolutionary factors approach, exaptation is one possible answer to the question “What evolutionary factors account for the form and distribution of this trait?”, and it appeals to a process of cooptation in contrast to a process of selection.

Buss and colleagues misleadingly discuss the sources or mechanisms of co-optations of structures, under their faulty definition, discussed above. In considering birds’ feathers, which were originally evolved for thermoregulation but subsequently co-opted for flight, they write “it is clearly natural selection that is responsible for transforming an existing structure into a new, modified structure with a different function” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 541). But Buss and colleagues have conflated two processes here. They’ve taken one process in which feathers, without physiological modification, were co-opted for flight through use (an exaptation), and confused it with another in which feathers were subsequently adaptively modified for enhanced flight capability (a secondary engineering adaptation, which has a function in both the etiological and design sense).

They object to Gould’s use of some mechanisms of co-optation, like cognitive capacities and motivational mechanisms, because they are clearly not cases of natural selection. They are at pains to distinguish current uses that are not “co-opted by natural selection” for their current uses from those that are naturally selected. But that is the whole point of introducing “exaptation.” Buss and colleagues fail to see that Gould does not require that the trait be “co-opted” by natural selection (which really means “selected,” based on their use of the term) in order to be an exaptation; this is a result of their own collapse of the two processes of exaptation and secondary adaptation.

Some measure of the responsibility for this confusion is Gould’s. His single misspeaking involving the term “function” in the 1991 paper was seized on by Buss and colleagues, and led them to search for an original function and a “distinct later function” in secondary adaptations, their “exaptations” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 541). When finding no later adaptive function, Buss and colleagues conclude that something is amiss. Moreover, when they understand exaptations as arising from earlier functions, they are missing half of the definition of exaptation, in which many traits with current uses are derived from traits with no adaptive function at all (i.e., spandrels).

But what turns on this confusion? The answer becomes clear in Buss and colleagues’ discussion of the evidence required to show that something is an exaptation. They require specification of (1) the original adaptation or by-product that was later coopted for the exaptation; (2) the causal mechanism responsible for the co-opting (e.g., on their account, natural selection or a selective motivational mechanism; note that they do not include any developmental constraints or mechanisms or nonselective factors); and (3) “the exapted biological function” of the trait, “that is, the manner in which it contributes to the solution to an adaptive problem of survival or reproduction” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 542).

Here, Buss and colleagues’ notion that an exaptation must have a biological function is doing some real work. As they put it, both the concepts of exaptation and adaptation invoke function, “therefore, both must meet the conceptual and evidentiary standards for invoking function.” It becomes clear that these standards are much too strict to bear the weight of what Gould and Vrba have defined as exaptations. Buss and colleagues write, for example, that the criteria for a proposed function include “the hallmarks of special design, including specialization of function, for solving a particular adaptive problem” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 546). Thus, it seems that Buss and colleagues are using Williams’ engineering definition of function and are mistakenly assuming that exaptations must exhibit this kind of function, whereas exaptations are actually demarcated precisely to avoid such a burden.

Buss and colleagues claim that selectionist explanations “would generally be necessary for explaining how functionless by-products are transformed into coopted spandrels that perform specific functions,” thus making complete their mistaken view of the connection between function and co-optation. In an adaptationist spin, all of this is used to defend their sought-for conclusion that natural selection is “the basic explanatory principle in biology” (Reference Buss, Haselton, Shackelford, Bleske and Wakefield1998, p. 543; emphasis added).

The key problem is that their view does not allow for exaptation to serve its original role in evolution, as a potential alternative evolutionary factor, since it has been defined away as a selective scenario, often involving stabilizing selection. Thus, the differences between the evolutionary psychologists Buss and colleagues, and Vrba and Gould are clear, as we can see from the Logic of Research Questions.

It is badly mistaken to read exaptations as examples of secondary adaptations subject to stabilizing selection. Because methodological adaptationists, like Buss and colleagues, ask the “function” research question, their question needs a function answer, thus producing a function-based definition of exaptation. This is incorrect. In sum, Gould’s single, misspoken mention of the ‘function’ of an exaptation in his Reference Gould1991 paper has enabled Buss and colleagues to completely reverse the intended meaning of ‘exaptation.’

A similar problem arises with evolutionary psychologists Reference Andrews, Gangestad and MatthewsAndrews et al. (2002a, Reference Andrews, Gangestad and Matthews2002b). In a paper in which they claim to define exaptation and propose definitive standards of evidence for adaptation and exaptation, they assume adaptations and functions for traits at the beginning of inquiry, proposing that all adaptive accounts must be eliminated as alternatives before a nonadaptive account may be seriously considered (Reference Andrews, Gangestad and MatthewsAndrews et al. 2002a p. 534; Reference Andrews, Gangestad and Matthews2002b p. 504). This approach suffers from similar faults as Buss et al.’s, but we won’t detail it here; analysis can be found in Reference Lloyd and GouldLloyd and Gould (2017).