Introduction
The influence of evolutionary history is well known to have resulted in major consequences for human health and disease (Benton et al. Reference Benton, Abraham, LaBella, Abbot, Rokas and Capra2021). Theoretical modelling has proposed that the most important factors influencing host-parasite coevolution are population dynamics and the genetic basis for infection, while other factors such as stochasticity (random effects) and whether time proceeds continuously or in discrete steps are also contributors (Buckingham and Ashby, Reference Buckingham and Ashby2021). The Stockholm Paradigm framework adds further complexity to this model by highlighting the role of climate change in triggering pathogen host-switching and ecological fitting (Brooks et al. Reference Brooks, Hoberg and Boeger2019).
Integrating evidence from a range of disciplines allows the application of our knowledge of parasite genetic origins and archaeological evidence for infection over time across the world (Ferreira et al. Reference Ferreira, Reinhard and Araújo2014; Mitchell, Reference Mitchell2015a, Reference Mitchell2023). When we couple this data with our understanding of variation in past human population dynamics, lifestyle, changes to the environment and ancient migrations (Mitchell, Reference Mitchell2024a), we will be in a position to explore the long and intimate association between people and parasites through time. The protozoan parasites to be investigated are malaria, leishmaniasis, trypanosomiasis and gastrointestinal pathogens such as Giardia, Entamoeba and Cryptosporidium. Helminths to be assessed include schistosomes, soil-transmitted nematodes such as whipworm, roundworm and hookworm, and a range of zoonotic tapeworms and flukes. The ectoparasites under scrutiny are fleas, head lice, body lice and public lice, as well as the bacterial pathogens they can transmit.
Human population dynamics through time
Changes in the number of people in a population and the density of people in a geographic area can be described through population dynamics (Henderson and Loreau, Reference Henderson and Loreau2019). Throughout most of human evolution, the population density is thought to have been extremely low. Despite this, early human species such as Homo erectus and later H. sapiens migrated out of Africa colonizing Europe, Asia, Australasia and Oceania, and subsequently the Americas (López et al. Reference López, van Dorp and Hellenthal2015). The population density seems to have started to increase in a meaningful way with the development of farming (the Neolithic period). Starting around 10 000 years ago, people developed herding of animals and cultivation of crops such as cereals in the Near East, rice, millet and sorghum in East Asia, and maize and squash in the Americas (Bellwood, Reference Bellwood2023). It has been proposed that farming provided foods that could be stored for consumption during predictable periods of resource shortages (such as winter) but could also save lives in times of unexpected scarcity following environmental disasters that might otherwise have led to a population crash (Boone, Reference Boone2002).
This led to some key changes that are sometimes referred to as the first epidemiological transition (Barrett et al. Reference Barrett, Kuzawa, McDade and Armelagos1998). Low-density hunter-gatherer groups caught and ate wild animals, which put them at risk of infection by the zoonotic parasite species they contained. Unless they chose to remain associated with an environmental asset such as a cave, such groups may have kept on the move in search of new food sources, leaving their faecal waste behind. In contrast, early farmers had to stay in one location to tend their crops (early urbanization), keeping them in contact with their faecal waste. The Neolithic period saw the domestication of certain species of wild animals such as sheep, goats, cattle, pigs and horses to become farm animals. Although hunting wild animals remained common in the Neolithic (Cummings and Harris, Reference Cummings and Harris2011), the wild component of the diet typically reduced over time into the Bronze Age and Iron Age. While this process meant a decreasing injury risk from hunting dangerous wild animals as they farmed their own herds, the risk of zoonotic parasite infection from wild animals was gradually taken over by the risk of zoonotic parasites from their farm animals (Ledger and Mitchell, Reference Ledger and Mitchell2022). This interpretation has been highlighted by the recent aDNA evidence indicating that the advent of herding in the Neolithic was associated with a notable increase in the infection of human populations by zoonotic bacterial pathogens (Sikora et al. Reference Sikora, Canteri, Fernandez-Guerra, Oskolkov, Ågren, Hansson, Irving-Pease, Mühlemann, Nielsen, Scorrano, Allentoft, Seersholm, Schoreder, Gaunitz, Stenderup, Vinner, Jones, Nystedt, Sjögren, Parkhill, Fugger, Racimo, Kristiansen, Iversen and Willerslev2025). For farmers, the combination of increased population size and density, coupled with sedentism and the resulting challenges with the disposal of faecal waste, appears to be a key factor leading to changes in parasitism in human evolution (Mitchell, Reference Mitchell2013). However, the way in which these changes affected parasite infection in early human populations seems to have varied in different regions of the world (Reinhard et al. Reference Reinhard, Ferreira, Bouchet, Sianto, Dutra, Iniguez, Leles, Le Bailly, Fugassa, Pucu and Araújo2013).
The second epidemiological transition is a term sometimes used to describe the shift away from infectious diseases towards the chronic diseases associated with industrialization (Barrett et al. Reference Barrett, Kuzawa, McDade and Armelagos1998). Industrialization allowed the development of large cities with even greater population size and density, initially resulting in the spread of gastrointestinal infectious diseases (Nagashima, Reference Nagashima2004; Davenport et al. Reference Davenport, Satchell and Shaw-Taylor2019). However, the development of science and technology resulted in an understanding of these pathogens and how they are spread, the development of sanitation infrastructure, clean water, techniques to keep food fresh for longer, synthetic crop fertilizers instead of using faecal waste, and medicines to clear parasite infection (Porter, Reference Porter1999). In consequence, most industrialized countries now have populations where parasite infection is very low, although the consequences of the more meagre industrial intestinal microbiome concern many (Sonneburg and Sonneburg, Reference Sonneburg and Sonneburg2019).
Early technologies and parasite risk
In the Mesolithic and Neolithic periods, humans developed technologies that made daily life easier for them. Examples of early technologies developed include sharper stone tools, pottery vessels, weaving equipment, housing, simple boats and crop irrigation (Baker, Reference Baker2018). While these technologies allowed early peoples to achieve their goals quickly or with less energy expenditure, some technologies had the potential to increase the risk of parasite infection. Weaving clothes would have made a safe home for ectoparasites such as fleas and body lice (Weiss, Reference Weiss2009). If clothes were shared with others, then those ectoparasites could spread too. While woven clothes would have been easier to wash than animal skins, it is likely that until such washing involved the use of hot water and soap-like substances, the potential for the washing process to reduce ectoparasites was probably limited.
A number of parasites, such as schistosomiasis and dracunculiasis, are spread when a host comes into contact with sources of warm, still freshwater. To complete their life cycles, these helminths require intermediate hosts that live in the water, such as snails for schistosomiasis and copepods for dracunculiasis (Galán-Puchades, Reference Galán-Puchades2020; Buonfrate et al. Reference Buonfrate, Ferrari, Adegnika, Stothard and Gobbi2025). Crop irrigation not only increases yields but also allows plants to be grown in regions where natural rainfall alone would be insufficient. Manmade irrigation systems appear to have been developed first by farmers in the Near East (Mesopotamia) about 7500 years ago (Helbaek, Reference Helbaek1972; Wilkinson, Reference Wilkinson1988). However, crop irrigation was later used by communities across the world, such as along the River Nile in Africa, and by those growing rice in Southeast Asia (Angelakis et al. Reference Angelakis, Zaccaria, Krasilnikoff, Salgot, Bazza, Roccaro, Jiminez, Kumar, Yinghua, Baba, Harrison, Garduno-Jimenez and Fereres2020). If the warm still fresh water became colonized by suitable intermediate hosts, and if an infected person from a different region entered the water and parasite larvae are released, then a new farming community could have become infected.
If early farmers dammed rivers or cut out cisterns from rock to create reservoirs to store water for crop irrigation or drinking in dry months of the year, this could have allowed them to live in regions where they might otherwise not be able. However, such locations act as suitable breeding grounds for mosquitoes. These mosquitoes had the potential to spread parasites such as malaria and lymphatic filariasis, as well as a range of viruses and bacteria (Dahmana and Mediannikov, Reference Dahmana and Mediannikov2020).
When humans developed early housing to shield themselves from the elements, they would have used whatever materials were available to them, with little idea as to whether the new environments they created would have made good homes for vectors that could transmit parasites to them. It has been argued that one of the factors leading to the significant prevalence of Chagas’ disease (Trypanosoma cruzi) in the prehistoric populations of Peru and Chile was colonization of the early dwellings made from wood and mud that created plenty of cracks where the triatomine bug vectors could hide (Rothhammer et al. Reference Rothhammer, Allison, Nuñez, Standen and Arriaza1985). The early earth ovens made by the populations of the Lower Pecos Canyonlands in Texas, USA, have also been proposed as locations where humans inadvertently created homes for triatomine bugs. The bugs could live in these baking pits and then intermittently feed on nearby people, so spreading Chagas disease there more than a thousand years ago (Reinhard and Araújo, Reference Reinhard and Araújo2015). Therefore, we can see that some early technologies might have clear advantages to early societies that developed them, while they would have been unaware of the health consequences from parasite infection that could then ensue.
Protozoan parasites
Malaria
In modern human populations, malaria is mainly caused by Plasmodium falciparum and P. vivax, with P. malariae, P. ovale and P. knowlesi making up the remainder (World Health Organization, 2024). Genetic analysis suggests that P. falciparum likely host switched from gorillas to humans in Africa around 60 000–40 000 years ago (Liu et al. Reference Liu, Li, Learn, Rudicell, Robertson, Keele, Ndjango, Sanz, Morgan, Locatelli, Gonder, Kranzusch, Walsh, Delaporte, Mpoudi-Ngole, Georgiev, Muller, Shaw, Peeters, Sharp, Rayner and Hahn2010; Otto et al. Reference Otto, Gilabert, Crellen, Böhme, Arnathau, Sanders, Oyola, Okouga, Boundenga, Willaume, Ngoubangoye, Moukodoum, Paupy, Durand, Rougeron, Ollomo, Renaud, Newbold, Berriman and Prugnolle2018). Arguments have been made that P. vivax host switched to humans from chimpanzees in Africa (Liu et al. Reference Liu, Li, Shaw, Learn, Plenderleith, Malenke, Sundararaman, Ramirez, Crystal, Smith, Bibollet-Ruche, Ayouba, Locatelli, Esteban, Mouacha, Guichet, Butel, Ahuka-Mundeke, Inogwabini, Ndjango, Speede, Sanz, Morgan, Gonder, Kranzusch, Walsh, Georgiev, Muller, Piel, Stewart, Wilson, Pusey, Cui, Wang, Farnert, Sutherland, Nolder, Hart, Hart, Bertolani, Gillis, LeBreton, Tafon, Kiyang, Djoko, Schneider, Wolfe, Mpoudi-Ngole, Delaporte and Peeters2014; Loy et al. Reference Loy, Liu, Li, Learn, Plenderleith, Sundararaman, Sharp and Hahn2017) or from macaques in Asia (Daron et al. Reference Daron, Boissière, Boundenga, Ngoubangoye, Houze, Arnathau, Sidobre, Trape, Durand, Renaud, Fontaine, Prugnolle and Rougeron2021). P. malariae is also thought to have originated in nonhuman primates in Africa and host switched to humans, although the species involved and timing are less clear (Rutledge et al. Reference Rutledge, Böhme, Sanders, Reid, Cotton, Maiga-Ascofare, Djimdé, Apinjoh, Amenga-Etego, Manske, Barnwell, Renaud, Ollomo, Prugnolle, Anstey, Auburn, Price, McCarthy, Kwiatkowski, Newbold, Berriman and Otto2017). Malaria has been shown to subsequently spread to the Americas with the transatlantic slave trade of the 1600s–1800s. Strains of falciparum malaria found in the areas of West Africa where the Portuguese obtained their slaves match the strains found in Portuguese colonies in South America (Brazil) today. Similarly, strains found in areas of West Africa where the Spanish obtained their slaves match those found in areas of the Americas previously administered by the Spanish (Caribbean, Mexico and northern parts of South America) (Yalcindag et al. Reference Yalcindag, Elguero, Arnathau, Durand, Akiana, Anderson, Aubouy, Balloux, Besnard, Bogreau, Carnevale, D’Alessandro, Fontenille, Gamboa, Jombart, Le Mire, Leroy, Maestre, Mayxay, Ménard, Musset, Newton, Nkoghé, Noya, Ollomo, Rogier, Veron, Wide, Zakeri, Carme, Legrand, Chevillon, Ayala, Renaud and Prugnolle2012). More recent work suggests that P. vivax was transferred to the Americas by European migrants from the 1500s onwards (Megan et al. Reference Megan, Skourtanioti, Pierini, Guevara, Mötsch, Kocher, Barquera, Bianco, Carlhoff, Bove, Freilich, Giffin, Hermes, Hiß, Knolle, Nelson, Neumann, Papac, Penske, Rohrlach, Salem, Semerau, Villalba-Mouco, Abadie, Aldenderfer, Beckett, Brown, Campus, Chenghwa, Berrocal, Damasek, Carlson, Durand, Ernée, Fântâneanu, Frenzel, Atiénzar, Guillén, Hsieh, Karwoski, Kelvin, Kelvin, Khokhlov, Kinaston, Korolev, Krettek, Küßner, Lai, Look, Majander, Mandl, Mazzarello, McCormick, de Miguel Ibáñez, Murphy, Németh, Nordqvist, Novotny, Obenaus, Olmo-Enciso, Onkamo, Orschiedt, Patrushev, Peltola, Romero, Rubino, Sajantila, Salazar-García, Serrano, Shaydullaev, Sias, Slaus, Stanco, Swanston, Teschler-Nicola, Valentin, Van de Vijver, Varney, Vigil-Escalera Guirado, Waters, Weiss-Krejci, Winter, Lamnidis, Prüfer, Nägele, Spyrou, Schiffels, Stockhammer, Haak, Posth, Warriner, Bos, Herbig and Krause2024).
Archaeological evidence for malaria can be found in preserved malarial DNA, antigens and in the skeletal changes of chronic anaemia (such as cribra orbitalia) caused by malaria. Malaria DNA is best preserved in regions where mummies survive, but it is occasionally recovered in human skeletal remains. As falciparum malaria originated in Africa, we might expect the earliest evidence to come from civilizations in Africa. Mummies from ancient Egypt and Nubia (Sudan), dating from 3200 BCE to 124 CE, have been found positive for P. falciparum using both immunoenzymatic assay and aDNA. If we include studies of both mummies and skeletons (221 individuals), 22% were positive. However, malarial DNA does not survive as well in ancient human skeletal remains compared with in mummified tissues, so if only studies of mummies are included (130 individuals), then 36% were positive (Mitchell, Reference Mitchell2024b).
A metagenomic study interrogating the previously sequenced genomes of over 10 000 ancient individuals from across the world has identified 36 early cases of malaria, which then underwent further enrichment. The most widely found species was P. vivax, being identified in Europe (Germany and Spain) and Asia (Russia) from the 4th–3rd millennium BCE (Neolithic period). P. falciparum was identified in Nepal dating to 804–765 BCE, and in Germany in 350–250 BCE (Iron Age). In the last 1000 years, many more cases of these 2 species were identified, as well as cases of P. malariae in Asia (Megan et al. Reference Megan, Skourtanioti, Pierini, Guevara, Mötsch, Kocher, Barquera, Bianco, Carlhoff, Bove, Freilich, Giffin, Hermes, Hiß, Knolle, Nelson, Neumann, Papac, Penske, Rohrlach, Salem, Semerau, Villalba-Mouco, Abadie, Aldenderfer, Beckett, Brown, Campus, Chenghwa, Berrocal, Damasek, Carlson, Durand, Ernée, Fântâneanu, Frenzel, Atiénzar, Guillén, Hsieh, Karwoski, Kelvin, Kelvin, Khokhlov, Kinaston, Korolev, Krettek, Küßner, Lai, Look, Majander, Mandl, Mazzarello, McCormick, de Miguel Ibáñez, Murphy, Németh, Nordqvist, Novotny, Obenaus, Olmo-Enciso, Onkamo, Orschiedt, Patrushev, Peltola, Romero, Rubino, Sajantila, Salazar-García, Serrano, Shaydullaev, Sias, Slaus, Stanco, Swanston, Teschler-Nicola, Valentin, Van de Vijver, Varney, Vigil-Escalera Guirado, Waters, Weiss-Krejci, Winter, Lamnidis, Prüfer, Nägele, Spyrou, Schiffels, Stockhammer, Haak, Posth, Warriner, Bos, Herbig and Krause2024). It should be noted that ancient Egypt was the only region of Africa included in the study, so we remain unsure of the date of host switching from non-human primates to humans in sub-Saharan Africa.
Analysis of the dental pulp of the teeth of 39 individuals from Versailles in northern France, dating to the 6th century CE (Merovingian period), has also detected malaria. ELISA detected Plasmodium antigens in 36% of individuals, with most infections being P. vivax, but some P. falciparum was also present (Boualam et al. Reference Boualam, Heitzmann, Mousset, Aboudharam, Drancourt and Pradines2023). Where genetic and antigen analysis are not possible, skeletal lesions commonly caused by chronic anaemia (such as cribra orbitalia) can sometimes be used as a proxy indicator for the presence of malaria in past populations, as malaria commonly leads to anaemia. Comparison of human skeletal remains of 5802 individuals from Anglo-Saxon England (410–1050 CE) found that those who lived in low-lying marshy regions were significantly more likely to have cribra orbitalia than those who lived at higher elevations where marshes were not present. It was argued that malaria, likely P. vivax, led to long-term anaemia in those who lived in the marshy regions, explaining the skeletal changes noted (Gowland and Western, Reference Gowland and Western2012).
Unlike most other parasites that affect humans, malaria has triggered the rise of a range of genetic mutations that reduce the risk of a person dying from infection. These include mutations to HbS, HbC, HbE, alpha and beta globin chains, glucose-6-phosphate dehydrogenase and Duffy-negative allele (Taylor et al. Reference Taylor, Parobek and Fairhurst2012). While being heterozygous for these mutations can reduce the risk of death from malaria, being homozygous will lead to death even in the absence of malaria in cases of sickle cell disease and thalassaemia. The driver for passing on these mutations may well be that malaria tends to kill infants and children (before they can reproduce and pass their genes on to the next generation), while those heterozygous for the mutation survive to adulthood and do pass on those genes to their offspring. Archaeological evidence for these gene mutations can be found in the Roman period. A child from the 5th century BCE cemetery at Lugano in Italy was found to have the gene mutation for glucose-6-phosphate dehydrogenase deficiency (G6PD med variant) (Sallares et al. Reference Sallares, Bouwman and Anderung2004). The genome of an individual from the 1st–3rd century necropolis at Monte Carru in Sardinia included the gene mutation for beta thalassaemia (Viganó et al. Reference Viganó, Haas, Rühli and Bouwman2017).
Chagas disease
Trypanosoma cruzi is spread to humans through the bite of triatomine bugs, and the infection is lifelong. Following a period of acute infection with fever, around 30–40% of people develop chronic disease with eventual death from cardiomyopathy, irregular heart rhythm and megaviscera, as dilated intestines can prevent swallowing or defecation (Pérez-Molina and Molina, Reference Pérez-Molina and Molina2018; Hochberg and Montgomery, Reference Hochberg and Montgomery2023). This zoonosis is only endemic to South and Central America, so it must have originated there.
Archaeological evidence takes the form of both mummies with signs of megaviscera, such as dilated heart and intestines, and ancient DNA. An autopsy study analyzed 35 mummies dating from 470 BCE to 600 CE from the Atacama Desert in northern Chile (although only 22 were in a good state). They found 41% demonstrated signs of megacolon, 9% had cardiomegaly and 4.5% had megaoesophagus (Rothhammer et al. Reference Rothhammer, Allison, Nuñez, Standen and Arriaza1985). If 30–40% of people infected today develop chronic disease with mega-syndromes, this might indicate that virtually everyone in the prehistoric population at Quebrada de Tarapacá had been infected. A more recent large study focused on aDNA to investigate 283 mummies from southern Peru and northern Chile, dating from 7050 BCE to 1800 CE. In the Chinchorro period (7050–3000 BCE), 39% of the 18 mummies tested were positive for T. cruzi aDNA. In the Chiribaya period mummies (1050–1250 CE), 47% of the 70 individuals were positive. In the Inca period mummies (1450–1550 CE), 50% of the 26 individuals were positive. If data for the entire group of 283 mummies from all time periods are amalgamated, the overall prevalence for infection was 40% (Aufderheide et al. Reference Aufderheide, Salo, Madden, Streitz, Buikstra, Guhl, Arriaza, Renier, Wittmers, Fornaciari and Allison2004). Bearing in mind that many of these samples are extremely ancient, this should be regarded as a minimum prevalence since some individuals may have been infected, but the trypanosome DNA did not survive well enough to be detected by the study. While the best ancient evidence for Chagas disease comes from the Atacama desert of Peru and Chile due to the large number of naturally preserved mummies there, trypanosomiasis appears to have been endemic in prehistoric populations throughout central America as well. For example, megacolon from Chagas disease has been identified in the mummy from a hunter-gatherer population from the Chihuahua Desert on the border between Texas and Mexico dating to 1150 years ago (Reinhard et al. Reference Reinhard, Fink and Skiles2003).
Leishmaniasis
Fossil protozoa from the genus Paleoleishmania have been identified in the gut of a sand fly trapped in Burmese amber dating to 100 million years ago, in the early Cretaceous period (Poinar and Poinar, Reference Poinar and Poinar2004; Poinar, Reference Poinar2007). A further example of Palaeoleishmania was found in a sand fly in amber from the Dominican Republic dating to 20–30 million years ago (Poinar, Reference Poinar2008). Leishmania is thought to have originated in the Gondwana supercontinent, and then, when the land mass broke up to form modern continents during the Jurassic period, further evolution of the parasite led to the different species we know today (Steverding, Reference Steverding2017). The modern forms that cause disease in humans are cutaneous, mucocutaneous and visceral leishmaniasis, which can be found in many tropical and subtropical regions of the world today where sand flies are endemic (World Health Organization, 2010, pp. 91–96; Pace, Reference Pace2014).
Archaeological evidence for leishmaniasis in past populations can be found in mummies, human skeletal remains and pottery sculptures. In mummies from ancient Egypt and Nubia (Sudan), aDNA analysis using PCR identified the kinetoplastid mitochondrial DNA of L. donovani (visceral leishmaniasis) (Zink et al. Reference Zink, Spigelman, Schraut, Greenblatt, Nerlich and Donoghue2006). In the 71 Nubian mummies, which dated from 550 to 1500 CE, 9 (12.9%) tested positive. Of the 91 Egyptian mummies, which dated to 2050–500 BCE, 4 tested positive. All of these 4 were from the Middle Kingdom, a time when there was regular trade between Egypt and Nubia. Egyptian mummies from earlier and later time periods were negative. Therefore, it was proposed that leishmaniasis was not endemic in ancient Egypt, but could be contracted by Egyptians who travelled to Nubia, where it was endemic (Zink et al. Reference Zink, Spigelman, Schraut, Greenblatt, Nerlich and Donoghue2006).
Further evidence for visceral leishmaniasis has been found in Italy, dating to the renaissance. Eleonora of Toledo (1522–1562) married into the politically powerful Medici family. Her skeletal remains were found to be positive for L. infantum using both PCR for the kinetoplastid mitochondrial DNA and a protein assay detecting IgG against L. infantum using Western blot gel electrophoresis. Autopsy performed by doctors immediately after her death reported enlarged liver and spleen, which we now know would be compatible with her visceral leishmaniasis (Nerlich et al. Reference Nerlich, Bianucci, Trisciuoglio, Schönian, Ball, Giuffra, Bachmeier, Pusch, Ferroglio and Fornaciari2012).
In South America, a different form of leishmaniasis appears to have infected the ancient populations (Novo et al. Reference Novo, Leles, Bianucci and Araujo2016). Human skeletal remains from San Pedro de Atacama in Chile, dating to around 1000 years ago, were noted to include individuals with destructive lesions to the nose and maxilla compatible with mucocutaneous leishmaniasis. aDNA was extracted from bone at the margins of the lesions, and the analysis indicated L. viannia (Costa et al. Reference Costa, Matheson, Lachetta, Llagostera and Appenzeller2009; Marstella et al. Reference Marstella, Torres-Rouff and Knudson2011). The prevalence of individuals with bony lesions was 0.5%, although the overall prevalence, including those with only soft tissue lesions, would be expected to be higher. Pottery sculptures from the 1st–8th century CE Moche (Mochica) culture from northern Peru include a good number with the appearance of destructive lesions of the nose that have the appearance of mucocutaneous leishmaniasis (Urteaga-Ballon, Reference Urteaga-Ballon, Ortner and Aufdeheide1991). The Inca civilization also appears to have been affected by mucocutaneous leishmaniasis. Analysis of 241 individuals from Makatampu in Peru dating to the 15th and 16th centuries CE showed 5 cases (2%) had destructive cranial lesions compatible with leishmaniasis (Altamirano Enciso et al. Reference Altamirano Enciso, Soares Moreira and Marzochi2001).
Gastrointestinal protozoa
Diarrhoeal illness can be triggered by a range of protozoa such as Entamoeba histolytica, Giardia duodenalis and Cryptosporidium spp. Genetic analyses have identified a variety of differing genotypes and interplay between human and non-human infection, but so far have not been able to fully understand the evolutionary origins of these protozoa (Weedall and Hall, Reference Weedall and Hall2011; Cui et al. Reference Cui, Li, Chen and Zhang2019; Ryan et al. Reference Ryan, Feng, Fayer and Xiao2021). However, archaeological evidence employing microscopy and ELISA has determined patterns that would indicate their origins.
Cryptosporidium sp. has been identified in 600–800 CE Mexico (Morrow and Reinhard Reference Morrow and Reinhard2016). Since tests for the organism have regularly been negative in early archaeological faecal samples from Europe and Asia, this would suggest the parasite may well have originated in the Americas. The earliest evidence for Entamoeba histolytica is from Greece during the Neolithic (5000–2000 BCE) (Le Bailly and Bouchet, Reference Le Bailly and Bouchet2006), and it has been found in many sites in Europe and the Near East during the Roman and medieval periods (Le Bailly et al. Reference Le Bailly, Maicher and Dufour2016; Wang et al. Reference Wang, Deforce, De Gryse, Eggermont and Mitchell2024). This would suggest that this is an Old World parasite, and since it is found in non-human primates in Africa, it may well have its origins there, before being spread worldwide by human migrations (Mitchell, Reference Mitchell2013; Steverding, Reference Steverding2025). The earliest evidence so far found for Giardia infection in humans is from 2 Iron Age latrines in Jerusalem dating to the 7th–6th century BCE (Mitchell et al. Reference Mitchell, Wang, Billig, Gadot, Warnock and Langgut2023). The most ancient written descriptions of diarrhoeal illness come from early texts from Mesopotamia dating to the 2nd and 1st millennium BCE. The Assyrian and Babylonian medical texts include descriptions such as ‘his stomach is colicky and has flowing of the bowels’, and ‘his insides are cramped, his bowels are loose’ (Scurlock and Andersen, Reference Scurlock and Andersen2005). While a range of bacteria and viruses can cause diarrhoeal illness, having shown that Giardia was present in the Near East in the first millennium BCE, this would indicate that a proportion of such cases may have been due to Giardia. It has been found at a range of Roman and medieval sites in Europe and the Near East (Williams et al. Reference Williams, Arnold-Foster, Yeh, Ledger, Baeten, Poblome and Mitchell2017; Ledger et al. Reference Ledger, Micarelli, Ward, Prowse, Carrol, Killgrove, Rice, Franconi, Tafuri, Manzi and Mitchell2021; Rabinow et al. Reference Rabinow, Wang, van Oosten, Meijer and Mitchell2024). Giardia has also been detected in a coprolite from a cave in Tennessee, USA, dating to 600–0 BCE (Faulkner et al. Reference Faulkner, Patton and Strawbridge Johnson1989). As Giardia is found in many different mammal species, it is possible that it spread around the world long ago and, as a zoonosis, was able to transfer between animals and humans wherever humans migrated.
Helminths
Schistosomiasis
Blood flukes of the Schistosoma genus infect a range of animals across the world, with some species damaging the urological system and others the gastrointestinal system. Genetic analysis of ribosomal RNA genes indicates an ancient origin in Asia and a basal lineage of Schistosoma japonicum (Attwood et al. Reference Attwood, Fatih, Mondal, Alim, Fadjar, Rajapakse and Rollinson2007). It has been proposed that during the middle Miocene (16–11 million years ago), mammals moved from Asia to Africa, transferring the genus there and allowing the development of S. mansoni and S. haematobium that affect humans and other primates (Lawton et al. Reference Lawton, Hirai, Ironside, Johnston and Rollinson2011). Schistosomes were only introduced into the Americas with the transatlantic movement of enslaved people from Africa to the New World between the 1600s and 1800s. Analysis of the genomes of S. mansoni in Africa with that of S. mansoni endemic in the islands of the French Caribbean indicates that the strains found in former French colonies in West Africa match those in the Caribbean (Crellen et al. Reference Crellen, Allan, David, Durrant, Huckvale, Holroyd, Emery, Rollinson, Aanensen, Berriman, Websoadter and Cotton2016). This spread was made possible by the presence of Biomphalaria glabrata freshwater snails in Caribbean islands that were physiologically close enough to the African intermediate host B. pfeifferi snails for S. mansoni to complete its life cycle (Morgan et al. Reference Morgan, Dejong, Snyder, Mkoji and Lokewr2001).
Archaeological evidence for schistosomiasis includes their eggs, antigens, aDNA and the skeletal changes of chronic anaemia. The earliest evidence so far identified dates from 4500 to 4000 BCE, from the site of Tell Zeidan in Syria (Anastasiou et al. Reference Anastasiou, Lorentz, Stein and Mitchell2014). This was an early farming settlement in the Euphrates River valley. An egg of a terminal spined schistosome was noted on microscopy of pelvic sediment of a child buried at the site, and subsequent aDNA analysis at the McMaster University Ancient DNA Laboratory identified 73 reads matching S. haematobium. Man-made crop irrigation systems were first developed in the Middle East around 5500 BCE to improve crop productivity (Helbaek, Reference Helbaek1972). As schistosomiasis can be contracted by people wading in fresh water where Bulinus sp. intermediate host snails are present, the development of crop irrigation appears to be amongst the earliest evidence so far for a manmade technology resulting in increased risk of infectious disease in humans (Mitchell, Reference Mitchell2023, p.19). Further evidence for early schistosomiasis in the Near East region comes from the ancient civilizations of Egypt and Nubia, where crop irrigation was used by farmers along the River Nile. The first ever published paleoparasitological study reported the eggs of S. haematobium during microscopic analysis of the kidneys of two out of three 20th Dynasty mummies (Ruffer, Reference Ruffer1910). Subsequent research employing microscopy, aDNA and ELISA for schistosome antigens in over 200 mummies has shown how widespread schistosomiasis appears to have been, with prevalence ranging from 10% to 65% in different populations (Mitchell, Reference Mitchell2024b).
In East Asia, the earliest evidence for oriental schistosomiasis comes from naturally preserved mummies from ancient China. For example, S. japonicum eggs have been identified in the Phoenix Hill mummy and the Changsha mummy in Hubei Province, both dating to the Han Dynasty (206 BCE-220 CE) (Yeh and Mitchell, Reference Yeh and Mitchell2016). Although the region’s schistosomiasis is named S. japonicum, this evidence would suggest that the disease did not originate in Japan but only spread there at a later date.
Soil-transmitted helminths
Whipworm (Trichuris trichiura) has been found in the faecal remains of most early human populations around the world, and Trichuris sp. is also found in non-human primates in Africa. Early archaeological examples in humans include 7800–7300 BCE Cyprus (Harter-Lailheugue et al. Reference Harter-Lailheugue, Le Mor, Vigne, Guilaine, Le Brun and Bouchet2005), 6410–6300 BCE Turkey (Ledger et al. Reference Ledger, Anastasiou, Shillito, Mackay, Bull, Haddow, Knusel and Mitchell2019a), 5840–5620 BCE Britain (Dark, Reference Dark2004) and 7830–7630 BCE Argentina (Fugassa et al. Reference Fugassa, Beltrame, Sardella, Civalero and Aschero2010). This would suggest that whipworm is an heirloom parasite that evolved in primates and early human ancestors in Africa and then spread around the world as humans migrated (Mitchell, Reference Mitchell2013).
The species of whipworm typically found in humans is very similar to T. suis, the form typically found in pigs. Pigs are known for coprophagy, where they eat their own faeces or those of other animals to gain nutrients from them (Soave and Brand, Reference Soave and Brand1991). This has the potential to act as a mode of spread for intestinal parasites. Genetic analysis of modern strains of whipworm in humans and pigs across the world has shown many similarities. However, the interpretation of the genetic differences identified indicates that when humans domesticated pigs, their similar physiology meant that pigs contracted human whipworm, probably in China. T. suis appears to have been spread around the world when humans transported infected pigs to other continents (Hawash et al. Reference Hawash, Betson, Al-Jubury, Ketzis, LeeWillingham, Bertelsen, Cooper, Littlewood, Zhu and Nejsum2016).
Roundworm (Ascaris lumbricoides) was present in humans from early prehistory, as demonstrated by palaeolithic evidence for human infection found in layers dated to 28 000–22 000 BCE in a cave at Arcy-sur-Cure in France (Bouchet et al. Reference Bouchet, Baffier, Girard, Morel, Paicheler and David1996). Roundworm eggs have also been recovered from the pelvic sediment of burials from China dating to 770–403 BCE (Wei et al. Reference Wei, Weng, Zhang, Fan and Xin2012), 620–290 BCE America (Fry, Reference Fry and Watson1974) and 6860–6740 BCE Brazil (Leles et al. Reference Leles, Araújo, Ferreira, Vicente and Iñiguez2008).
Infections by roundworms in humans and pigs share many similarities. Some have argued that A. lumbricoides and A. suum are the same species (Leles et al. Reference Leles, Gardner, Reinhard, Iñiguez and Araújo2012), and genetic analyses indicate that they represent a genetic complex with considerable hybridization (Easton et al. Reference Easton, Gao, Lawton, Bennuru, Khan, Dahlstrom, Oliveira, Kepha, Porcella, Webster, Anderson, Grigg, Davis, Wang and Nutman2020). In the same way that occurred with whipworm, it seems likely that Ascaris lumbricoides originated in primates and early humans in Africa, spread around the world with early human migrations and switched hosts to pigs once they were domesticated by humans (Mitchell, Reference Mitchell2013).
Hookworms (Ankylostoma duodenalis and Necator americanus) produce fragile eggs that do not survive as well in archaeological contexts as do the robust eggs of helminths such as Ascaris, Trichuris and Taenia. However, they have been identified in some early societies, such as in Chile, Brazil and Argentina, dating to several thousand years ago (Gonçalves et al. Reference Gonçalves, Araújo and Ferreira2003). Necator and Ancylostoma infect gorillas, chimpanzees, baboons and a range of monkeys in Africa (Seguel and Gottendker, Reference Seguel and Gottendker2017). This would suggest that hookworm is an heirloom parasite that has infected humans throughout our evolution (Mitchell, Reference Mitchell2013).
Lifestyle has been identified as having a significant effect upon infection rates by whipworm, roundworm, hookworm and pathogenic amoebae. Modern research has shown that when nomadic hunter-gatherer groups settle to take up farming, all these intestinal parasites become much more common (Dounias and Froment, Reference Dounias and Froment2006). The same pattern is seen in past populations, where from the Bronze Age onwards zoonotic parasites from eating wild animals become less common, and helminths spread by poor sanitation, such as whipworm and roundworm, are much more widespread (Reinhard et al. Reference Reinhard, Ferreira, Bouchet, Sianto, Dutra, Iniguez, Leles, Le Bailly, Fugassa, Pucu and Araújo2013; Yeh and Mitchell, Reference Yeh and Mitchell2016; Mitchell, Reference Mitchell2017). In the Americas, pinworm has also been shown to become much more widespread with the development of farming and crowded settlements with communal sleeping arrangements (Camacho and Reinhard, Reference Camacho and Reinhard2020).
Infections with high worm burdens of whipworm, roundworm and hookworm may cause chronic anaemia, abdominal cramps, diarrhoea and affect growth in children (Jourdan et al. Reference Jourdan, Lamberton, Fenwick and Addiss2018). Therefore, we would expect these parasites to have had a considerable impact upon those living in past civilizations across the world that practised farming, underwent urbanization and experienced increasing population density (Mitchell, Reference Mitchell2023).
Taenia tapeworms
Taenia are contracted by humans when they consume raw or undercooked meat. T. solium and T. asiatica are transmitted in pork, while T. saginata is transmitted in beef. These species are specific to the human host, but understanding their relationship with other species of Taenia can help determine their origins. Molecular phylogenetic studies indicate that T. saginata and T. asiatica are closely related to species of Taenia that infect hyenas in Africa, while T. solium is more closely related to T. arctos, which infects brown bears. Therefore, it has been suggested that beef and Asiatic tapeworms in humans probably originated in Africa, while pork tapeworm may have originated separately in Asia (Terefe et al. Reference Terefe, Hailemariam, Menkir, Nakao, Lavikainen, Haukisalmi, Iwaki, Okamoto and Ito2014). Comparison of the genomes of T. saginata and T. asiatica has estimated that the 2 species diverged around 1.1 million years ago. Therefore, T. saginata may have been carried to Asia from Africa by migrating archaic humans (such as Homo erectus), becoming introduced to wild pig populations there, and evolving into T. asiatica (Wang et al. Reference Wang, Wang, Luo, Xiao, Luo, Gao, Dou, Zhang, Guo, Meng, Hou, Zhang, Zhang, Yang, Meng, Mei, Li, He, Zhu, Tan, Zhu, Yu, Cai, Zhu, Hu and Ca2016). The archaeological evidence supports such a hypothesis, as Taenia eggs have been recovered in human contexts from ancient Egypt and Nubia in Africa (Mitchell, Reference Mitchell2024b) as well as across Europe and Asia in prehistory (Anastasiou, Reference Anastasiou and Mitchell2015; Seo and Shin, Reference Seo, Shin and Mitchell2015).
Fish tapeworms
Broad tapeworms (Diphyllobothriidae) affecting humans can be caused by a range of species in different regions of the world, including those in the genus Dibothriocephalus, Diphyllobothrium and Adenocephalus. They are contracted by eating raw, smoked, pickled, dried or undercooked fish. These parasites can infect a range of fish-eating mammals and birds as well as humans (Scholz et al. Reference Scholz, Kuchta and Brabec2019). Archaeological evidence for fish tapeworm infection in human faeces has been found in early societies in Africa, Europe, Asia and the Americas, indicating that humans have been at risk of infection throughout our history (Le Bailly and Bouchet, Reference Le Bailly and Bouchet2013). Both geography and dietary preferences had a significant impact on transmission in past societies. Those species relying on freshwater fish for their life cycle (such as Dibothriocephalus dendriticus and D. latus) were much more common throughout history in well-watered regions of northern Europe compared with the hotter, drier regions of southern Europe (Knorr et al. Reference Knorr, Smith, Ledger, Clapés, Peña-Chocarro and Mitchell2019). Trends in fish tapeworm infection over time have also been noted. It was relatively widespread in Europe during the Neolithic and Bronze Age when people had a mixed diet from farming and hunting wild foods, but then it appears to have been less common as parasites spread by poor sanitation dominated during the Roman Period, before becoming more common again in the medieval period (Ledger et al. Reference Ledger, Murchie, Dickson, Kuch, Haddow, Knusel, Stein, Parker Pearson, Ballantyne, Knight, Deforce, Carroll, Rice, Franconi, Sarkic, Redzic, Rowan, Cahill, Poblome, de Fatima Palma, Bruckner, Mitchell and Poinar2025). In the medieval period, fish tapeworm infection was noteworthy in populations living along the river systems of northern Europe (Rocha et al. Reference Rocha, Harter-Lailheugue, Le Bailly, Araujo, Ferreira, Serra-Freire and Bouchet2006; Yeh et al. Reference Yeh, Pluskowski, Kalējs and Mitchell2014; Graff et al. Reference Graff, Jones, Bennion-Peddley, Ledger, Deforce, Degraeve, Byl and Mitchell2020; Rabinow et al. Reference Rabinow, Wang, van Oosten, Meijer and Mitchell2024). These trends over time might reflect changes in preferences for eating freshwater fish compared with sea fish, or the consumption of fish in medieval Europe on fast days when meat consumption was not permitted by the catholic church (Mitchell Reference Mitchell2015b).
Liver flukes
A variety of flukes are known to have infected past human populations, such as the intestinal fluke Echinostoma in Bronze Age Britain and medieval Belgium (Ledger et al. Reference Ledger, Grimshaw, Fairey, Whelton, Bull, Ballantyne, Knight and Mitchell2019b; Rabinow et al. Reference Rabinow, Deforce and Mitchell2023), Fasciolopsis buski in Ming Dynasty China (Yeh and Mitchell, Reference Yeh and Mitchell2016) and the lung flukes Paragonimus and Metagonimus in the first millennium CE Korea and Japan (Matsui et al. Reference Matsui, Kenehara and Kenehara2003; Seo et al. Reference Seo, Oh, Hong, Chai, Cha, Bang, Cha, Wi, Park and Shin2017). However, here we will consider the group of flukes that have evolved to infect the liver, as they are linked with a number of fascinating stories (Wang and Mitchell, Reference Wang and Mitchell2022).
Some are contracted by eating raw or undercooked freshwater fish, the most important being Chinese liver fluke (Clonorchis sinensis), Southeast Asian liver fluke (Opisthorchis viverrini) and Cat liver fluke (O. felineus). Others are contracted by eating plants where the intermediate form of the parasite is located, such as sheep liver fluke (Fasciola hepatica), giant liver fluke (F. gigantica) and the lancet liver fluke (Dicrocoelium dendriticum) (Harrington et al. Reference Harrington, Lamberton and McGregor2017). All these flukes are zoonoses that infect wild mammals, but were also able to infect humans when early migrations led them out of Africa to regions of the planet where these helminths are endemic.
Many have speculated over the years that the 2000-year-old Silk Route from China to the Eastern Mediterranean might have been responsible for the spread of infectious diseases (Monot et al. Reference Monot, Honoré, Gernier, Zidane, Sherafi, Painz-Mondolfi, Matsuoka, Taylor, Donoghue, Bouwman, Mays, Watson, Lockwood, Khamesipour, Dowlati, Jianping, Rea, Vera-Cabrera, Stefani, Banu, Macdonald, Sapkota, Spencer, Thomas, Harshman, Singh, Busso, Gattiker, Rougemont, Brennan and Cole2009; Simonson et al. Reference Simonson, Okinaka, Wang, Easterday, Huynh, U’Ren, Dukerich, Zanecki, Kenefic, Beaudry, Schupp, Pearson, Wagner, Hoffmaster, Ravel and Keim2009; Schmid et al. Reference Schmid, Büntgen, Easterday, Ginzler, Walløe, Bramanti and Stenseth2015). However, the first archaeological proof we have for the movement of people along the Silk Route with pathogens is that of the Chinese liver fluke. The Silk Route was established during the Han Dynasty, and numerous relay stations were constructed to act as accommodation for government officials and provide a change of horses for the postal service (Hansen, Reference Hansen2012). Xuanquanzhi relay station dates from 111 BCE to 109 CE, and was located at Dunhuang, in the arid northwest of China (He, Reference He2000). Being next to the Taklamakan Desert, the area is so dry that the personal hygiene sticks recovered from excavation of its latrines still have cloth and dried faeces adherent to them. Microscopy showed the eggs of roundworm, whipworm, Taenia tapeworm and Chinese liver fluke. The closest regions of China with wetlands where the Chinese liver fluke could complete its life cycle are 1500 km away from Dunhuang. This indicates that someone who used the latrine at this relay station as they travelled the Silk Route had previously eaten raw or undercooked fish in eastern or southern China, when they must have become infected with the liver fluke (Yeh et al. Reference Yeh, Mao, Wang, Qi and Mitchell2016).
Chinese liver fluke has also been involved with transoceanic migrations. In the 1800s, a shortage of manual labour on the west coast of America led to migrants from China travelling across the Pacific to work in hotels, laundries and farms. Wong Nim was a businessman of Chinese ancestry who, in 1900, owned property in San Bernardino in California, where he housed Chinese migrants. Analysis of the latrines there showed the eggs of roundworm, whipworm and Chinese liver fluke (Reinhard et al. Reference Reinhard, Araújo, Sianto, Costello and Swope2008). As the type of water snails required for the Chinese liver fluke to complete its life cycle are not present in the Americas, the fluke could not become endemic there. However, the presence of the eggs in a property associated with Chinese migrants acts as a record of this long-distance migration.
Cat liver fluke eggs have been recovered at a series of archaeological sites in northern Siberia (Russia) during the medieval period onwards, indicating the consumption of raw or undercooked fish by the populations living there (Slepchenko et al. Reference Slepchenko, Bugmyrin, Kozlov, Vershubskaya and Shin2019). One intriguing site is that of Stadukhinsky Fort in eastern Siberia, which dates from the 17th and 18th centuries. This fort was located at a summer port so fur trappers could export their animal furs before the winter ice cut off the sea route. The appearance of the Opisthorchiidae eggs found at its excavation would be compatible with either the cat liver fluke or the Chinese liver fluke. Cat liver fluke is endemic in western Siberia but not eastern Siberia. If these eggs were those of a cat liver fluke, it would indicate the migration of trappers and sailors from western Siberia to eastern Siberia to staff the fort. However, Chinese pottery, smoking pipes and other material culture were recovered during the fort’s excavation. If Chinese merchants came to trade at the fort, or if Russians headed south to trade in China, it is possible that these Opisthorchiidae eggs represent the Chinese liver fluke (Slepchenko et al. Reference Slepchenko, Lobanovam, Vizgalov, Alyamkin and Ivanov2022).
Ectoparasites
Fleas, head lice, body lice and pubic lice have infected humans and their ancestors through deep time. Some of these have the ability to transmit pathogens that have led to major health consequences for past societies. Genome sequencing leads to estimations that around 11.5 million years ago, the lineage that would become the human pubic louse (Pthirus pubis) diverged from an ancestor of the chimpanzee and human body louse and head louse in Africa. The lineage that would later become the human body louse (P. humanus) is thought to have diverged from the chimpanzee body louse (P. schaeffi) around 5.6 million years ago (Reed et al. Reference Reed, Smith, Hammond, Rogers and Clayton2004). Different lineages (clades) of head lice are found in different geographic regions, which has been interpreted to indicate that one lineage was spread from Africa by archaic human species (such as Homo erectus) before modern humans (H. sapiens) evolved and spread with their own lice lineages (Reed et al. Reference Reed, Smith, Hammond, Rogers and Clayton2004; Light et al. Reference Light, Allen, Long, Carter, Barrow, Suren, Raoult and Reed2008; Boutellis et al. Reference Boutellis, Abi-Rached and Raoult2014). The potential effect of the introduction of clothing by early modern humans upon the success of body lice has also been considered (Weiss, Reference Weiss2009).
The prevalence of head lice in past populations has been estimated from careful examination of the scalp and hair of mummies. One project looked at 218 mummies from Wadi Halfa in ancient Nubia (Sudan), dating from 350 to 550 CE, and found that 40% were positive for head lice (Armelagos, Reference Armelagos1969). In prehistoric Peru, 79% of 63 Chinchorro period mummies (3000–1000 BCE) were positive for head lice (Arriaza et al. Reference Arriaza, Standen, Reinhard, Araújo, Heukelbach and Dittmar2013), and 44% of 75 Chiribaya period mummies (1000–1250 CE) were positive (Reinhard and Buikstra, Reference Reinhard and Buikstra2003). This highlights how widespread head lice must have been in ancient cultures.
Human fleas (Pulex irritans) and body lice have been shown to be efficient transmitters of Yersinia pestis, the pathogen responsible for bubonic plague (Bland et al. Reference Bland, Long, Rosenke and Hinnebusch2024). Plague genomes from the Neolithic dating to around 3000 BCE do not appear to have the necessary features for flea-based transmission (Susat et al. Reference Susat, Lübke, Immel, Brinker, Macãne, Meadows, Steer, Tholey, Zagorska, Gerhards, Schmölcke, Kalnins, Franke, Petersone-Gordina, Teßman, Tõrv, Schreiber, Andree, Berzins, Nebel and Krause-Kyora2021), but the ymt flea adaptation locus was present by the Bronze Age (Spyrou et al. Reference Spyrou, Tukhbatova, Wang, Valtueña, Lankapalli, Kondrashin, Tsybin, Khokhlov, Kühnert, Herbig, Bos and Krause2018; Valtueña et al. Reference Valtueña, Neumann, Spyrou, Musralina, Aron, Beisenov, Belinskiy, Bos, Buzhilova, Conrad, Djansugurova, Dobes, Ernée, Fernández-Eraso, Frohlich, Furmanek, Haluszko, Hansen, Harney, Hiss, Hübner, Key, Khussainova, Kitov, Kitova, Knipper, Kühnert, Lalueza-Fox, Littleton, Massy, Mittnik, Mujika-Alustiza, Olalde, Papac, Penske, Peska, Pinhasi, Reich, Reinhold, Stahl, Stäunle, Tukhbatova, Vasilyev, Veselovskaya, Warinner, Stockhammer, Haak, Krause and Herbig2022). Moving between wild rodent reservoirs and human populations, plague has resulted in at least 3 worldwide pandemics: the Plague of Justinian in the 6th century CE, the Black Death in the 14th century and the third pandemic from the late 19th century (Barbieri et al. Reference Barbieri, Signoli, Chevé, Costedoat, Tzortzis, Aboudharam, Raoult and Drancourt2021).
Another pathogen spread by human ectoparasites is that of Borrelia recurrentis, which causes louse-borne relapsing fever. This spirochaete is spread when the human body louse feeds or when its faeces are rubbed into areas of broken skin. Untreated fatality rates can reach 40% in some epidemics (Warrell, Reference Warrell2019). Ancient DNA analysis of human skeletal remains has identified cases of B. recurrentis across Asia dating back to 3000 BCE, becoming fairly widespread in Europe during the medieval period (Sikora et al. Reference Sikora, Canteri, Fernandez-Guerra, Oskolkov, Ågren, Hansson, Irving-Pease, Mühlemann, Nielsen, Scorrano, Allentoft, Seersholm, Schoreder, Gaunitz, Stenderup, Vinner, Jones, Nystedt, Sjögren, Parkhill, Fugger, Racimo, Kristiansen, Iversen and Willerslev2025).
Individuals buried in a medieval mass grave at Bondy in France have been analyzed for the aDNA of pathogens to determine the cause of the fatalities. Of 14 skeletons whose teeth were tested, 2 were positive for the aDNA of Yersinia pestis, making it likely that the mass grave dates to a bubonic plague outbreak. Interestingly, 3 individuals were positive for Bartonella quintana, the bacteria that cause trench fever, which is spread by the bites of body lice (Tran et al. Reference Tran, Forestier, Drancourt, Raoult and Aboudharam2011a). Further work by the same team studied 173 individuals from mass graves dating to the 14th and 16th centuries from Venice, Italy. Y. pestis aDNA was identified in 3 individuals and B. quintana in 5 individuals (Tran et al. Reference Tran, Signoli, Fozzati, Aboudharam, Raoult and Drancourt2011b). Such findings highlight how ectoparasites were spreading multiple bacterial pathogens in medieval and renaissance Europe.
Head lice have been found trapped between the teeth of Roman-period wooden combs recovered from the Dead Sea and Judean Desert in Israel. A study analysing the aDNA of 24 such head lice identified Acinetobacter baumannii in 3 of them (12.5%) (Amanzougaghene et al. Reference Amanzougaghene, Mumcuoglu, Fenollar, Alfi, Yeslyurt, Raoult and Mediannikov2016). Infection by this bacterium can cause fevers, sweats, a rash and septicaemia, and is a challenging cause of multidrug resistant hospital acquired infection today (Antunes et al. Reference Antunes, Visca and Towner2014).
Body lice were extracted from mass graves of French soldiers dug at Vilnius in Lithuania during their retreat from Russia in 1812 during the Napoleonic Wars. Of 5 lice recovered, 3 were found positive for the aDNA of Bartonella quintana (trench fever). Thirty-five burials of French soldiers underwent DNA analysis of their teeth. Seven were positive for B. quintana, and three were positive for Rickettsia prowazeckii, which causes epidemic typhus (Raoult et al. Reference Raoult, Dutour, Houhamdi, Jankauskas, Fournier, Ardagna, Drancourt, Signoli, Dang La, Macia and Aboudharam2006). Such results highlight how human ectoparasites have acted as significant vectors for the spread of bacterial pathogens at major events throughout history.
Conclusion
Here, we have explored the evidence showing how there has been a long and intimate association between humans and parasites throughout our evolution. It can be seen that a range of heirloom parasites infected early humans and non-human primates, while other zoonotic parasites host switched from a range of mammals to humans as early people migrated to new regions of the planet. This interconnectedness between humans and other animals remains a focus for the One Health approach to medicine today. Changes in lifestyle associated with the 3 epidemiological transitions had major impacts on the risk of parasite transmission to and between our ancestors. Mobile hunter-gatherers, settled farmers, urbanized town-dwellers and modern industrialized societies all experienced different patterns of parasite infection. Early technologies allowed humans to live in new regions and protected them against environmental catastrophes such as droughts and crop failures, but sometimes these technologies also allowed new parasite species to become introduced in those societies. We can track how past human migrations have moved parasites around the planet by exploring genetic variation in modern parasites and also assessing patterns in space and time in the archaeological evidence for key species. Where they were endemic, protozoan parasite infections such as malaria, leishmaniasis and Chagas disease likely caused a greater disease burden to early societies than did intestinal helminths. In contrast to the relatively mild health impact of human ectoparasites themselves, from the Bronze Age we see how bacterial pathogens utilized ectoparasites to infect millions of humans over the millennia, leading to numerous deaths from a range of epidemic diseases such as bubonic plague, louse-borne relapsing fever, trench fever and epidemic typhus. The burden of parasite infection upon the success of ancient civilizations seems to have been notable, and helps us to understand the ways in which parasites have moulded human history.
Author’s contribution
This review is all the work of Piers Mitchell
Financial support
None
Competing interests
None
Open access
