Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans

Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans

Quaternary International xxx (2016) 1e8 Contents lists available at ScienceDirect Quaternary International journal homepage: www.elsevier.com/locate...

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Quaternary International xxx (2016) 1e8

Contents lists available at ScienceDirect

Quaternary International journal homepage: www.elsevier.com/locate/quaint

Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans George H. Perry a, b, *, Paul Verdu c a

Department of Anthropology, Pennsylvania State University, University Park, PA 16802, USA Department of Biology, Pennsylvania State University, University Park, PA 16802, USA c CNRS, MNHN, Universit e Paris Diderot, Sorbonne Paris Cit e, UMR 7206 Eco-Anthropology and Ethno-Biology, Paris 75016, France b

a r t i c l e i n f o

a b s t r a c t

Article history: Available online xxx

We review contributions from the field of genomics that have helped to inform our understanding of the history and evolutionary ecology of tropical rainforest hunting and gathering behavior by humans, and discuss potential opportunities for future studies. This perspective encompasses i) the question of the antiquity of full-time tropical rainforest occupation, ii) the characterization of biological adaptations to the particular ecological challenges of this habitat, including small adult body size or the “pygmy” phenotype, and iii) the timing and nature of interactions between hunter-gatherer groups and the farming populations that migrated into interior tropical rainforest habitats following the origins of agriculture. © 2016 Elsevier Ltd and INQUA. All rights reserved.

Keywords: Human population history Human evolutionary ecology Hunter-gatherers Population genomics Polygenic adaptation Population admixture

1. Introduction Our aim is to highlight three areas in which genomics-based analyses have thus far informed our understanding of the history and evolutionary ecology of the human peopling of tropical rainforests, or may have future potential to do so. First, when did human populations living in tropical rainforests today first settle these environments on a full-time basis? While archaeological records show that humans did occupy tropical rainforests in both Central Africa and Asia tens of thousands of years prior to the origins of agriculture in those regions (Cornelissen, 2002; Mercader, 2002; Piper and Rabett, 2009; Perera et al., 2011; Roberts et al., 2015), whether the occupation was transient or full-time, and the relationships of those populations to modern rainforest inhabitants, are not fully understood. Even as paleoanthropologists have stepped back somewhat from a strict savannah-based view of human origins in Africa to consider the possibility of more complex and diverse hominin habitats (Vrba, 2007; Cerling et al., 2011; Dominguez-Rodrigo, 2014; Marean et al., 2015), the tropical rainforest environment is still distinct from those typically envisioned for most of hominin evolutionary history. This habitat poses particular challenges to

* Corresponding author. Department of Anthropology, Pennsylvania State University, University Park, PA 16802, USA. E-mail addresses: [email protected] (G.H. Perry), [email protected] (P. Verdu).

human hunter-gatherers, with high heat and humidity (CavalliSforza, 1986), high structural density (Diamond, 1991), high densities of certain pathogens (Guernier et al., 2004), and low food availability especially in certain seasons (Hart and Hart, 1986). Against this backdrop, the timing of the first shift to full-time rainforest hunter-gatherer behavior is uncertain. In fact, given the severity of food scarcity, scholars have debated whether year-round occupation is even possible without agricultural trade (e.g., Hart and Hart, 1986; Headland, 1987; Bailey et al., 1989; Bahuchet et al., 1991; Colinvaux and Bush, 1991; Dwyer and Minnegal, 1991; Endicott and Bellwood, 1991; Headland and Bailey, 1991; Sato, 2001; Yasuoka, 2006). In the section Population Divergence we discuss genomic data and analyses that may help to ultimately resolve this debate. Understanding the antiquity of full-time rainforest occupation (and the cultural context thereof) is a critical input to our second topic e how might human rainforest hunter-gatherer populations have adapted biologically to their challenging habitat? Specifically, ecological interpretations of hypothesized adaptations to tropical rainforest habitats, such as small adult body size or the ‘pygmy’ phenotype (Perry and Dominy, 2009), could vary widely depending on whether the ancestors of these populations faced the rainforest's ecological constraints for tens of thousands of years prior to their interactions with agriculturalists and the associated availability of cultivated foods. Regardless, as discussed in the section Ecological Adaptations to the Rainforest there is strong potential

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Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038

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from the combination of evolutionary genomic analyses and genotypeephenotype association studies to both test existing hypotheses concerning putative rainforest hunter-gatherer biological adaptations and to develop wholly new hypotheses. Doing so will represent a major advance in our understanding of the evolutionary and ecological histories of these populations. Third, following the development of agriculture, what was the nature of interaction between rainforest hunter-gatherers and agriculturalists spreading into rainforest environments? Ethnologists have extensively studied the typically complex cultural and socioeconomic interactions among rainforest hunter-gatherer populations and their agricultural neighbors (Bahuchet and Guillaume, 1982; Headland and Reid, 1989; Hill and Hurtado, 1996; Joiris, 2003; Rupp, 2014; Takeushi, 2014). However, ethnographic methods alone cannot investigate the history of such interactions beyond several generations in the past. Furthermore, with archaeological approaches alone it is challenging to reliably associate cultural changes observed in the past to a history of interaction among huntergatherer and agricultural rainforest populations (e.g., Oslisly et al., 2013). Thankfully, population genomic analyses have much to contribute in this area. In the section Rainforest hunter-gatherer interactions with agriculturalists, we describe how population genetic approaches have helped to identify and characterize the prehistoric encounters between agriculturalist and hunter-gatherer populations in tropical rainforest environments, including empirical estimates of the amount of genetic admixture between these groups, the identification of sex biases in the pattern of admixture, and variation in the timing of admixture across different regions. We note that because the hunter-gatherer/agriculturalist subsistence distinction tends to be considerably less marked for populations presently inhabiting the tropical rainforests of South America (Roosevelt, 1998), our review is focused on Africa and Asia (and with the greatest emphasis on Africa due to the more extensive history of rainforest hunter-gatherer population genetic studies in that continent). Ultimately, consideration of the evolutionary histories and subsistence system dynamics of South American rainforest populations may aid the resolution of questions concerning the similar habitats in Africa and Asia. At the present time, however, this opportunity is outside the scope of our review. 2. Population divergence The vertical, parent-to-child inheritance of DNA allows population geneticists to reconstruct coalescent histories of the genetic variants observed among human individuals and populations (e.g., Nordborg, 2001). Based on this paradigm, numerous statistical approaches have been developed to estimate the dates of past population divergences (i.e., when groups of individuals ceased to randomly mate in the population history), quantify the level of gene flow between populations, and characterize population size changes over time. The recent availability of large, genomic-scale datasets has facilitated reconstructions of the otherwise unknown demographic histories of rainforest hunter-gatherer populations at different geographical scales. At the worldwide scale, populations who traditionally hunted and gathered in tropical rainforests are, on average across the genome, genetically more similar to other populations from the same continent (e.g., Africa and Asia), including agriculturalist populations, than they are to the rainforest hunter-gatherer populations from other continents (Rasmussen et al., 2011; Migliano et al., 2013). This result, along with the low likelihood that the routes of MiddleeLate Pleistocene modern human dispersal(s) Out of Africa (Ramachandran et al., 2005; Li et al., 2008; Henn et al., 2012; Reyes-Centeno, in press) could have exclusively followed tropical rainforest habitats, suggests that full-

time occupation of tropical rainforest habitats occurred independently in the African and Asian continents. At the intra-continent scale, population genomic analyses have discovered that all African rainforest hunter-gatherer populations share a more recent common origin with each other relative to their more ancient divergence with their respective neighboring agricultural populations (Patin et al., 2009; Verdu et al., 2009; Batini et al., 2011). Specifically, estimates of the divergence between African rainforest hunter-gatherer and Bantu-speaking agriculturalist populations range from ~60,000 to ~90,000 BP (Patin et al., 2009; Verdu et al., 2009; Hsieh et al., 2016), versus a divergence of ~20,000 BP between rainforest hunter-gatherer populations from West Central and East Central Africa (Patin et al., 2009). Within these regions, rainforest hunter-gatherer groups in West Central Africa diverged relatively recently from their common ancestor (~2900 BP; Verdu et al., 2009; Batini et al., 2011) whereas the BaSua (very often also called BaMbuti) and BaTwa populations from East Central Africa (the Democratic Republic of Congo and Uganda, respectively) are genetically more distinct from one another (Patin et al., 2014), although the date of their divergence has not yet been estimated. At the within-Asian continent scale, the picture of ancestral population divergence is currently less clear. The results from at least some population genomic analyses suggest that the rainforest hunter-gatherer groups in the region do not likely all share a common ancestor to the exclusion of modern agricultural populations. Specifically, the population histories of rainforest huntergatherer groups from the Philippines, Malaysia, and the Andaman Islands appear distinct from one another relative to more closely neighboring populations (Abdulla et al., 2009; Pugach et al., 2013; Aghakhanian et al., 2015). However, there is also considerable evidence suggesting a complex history of ancient population interaction and recent histories of admixture that are not fully understood, and that complicate analyses (Reich et al., 2011; Scholes et al., 2011; Jinam et al., 2012; Migliano et al., 2013; Pugach et al., 2013; Aghakhanian et al., 2015). Specific divergence time estimates between rainforest hunter-gatherer populations and their most closely related agricultural neighbors are relatively recent, for example ~4000e6000 BP for Malaysian groups (Deng et al., 2014), although the same caveat concerning the potential complications of unresolved admixture history also applies here. The genomic-based estimates of population divergence times are simply not informative with respect to the open question about the origins of full-time rainforest occupation, as the transition to this habitat could have occurred anytime subsequent to divergence of the proto-rainforest hunter-gatherer agriculturalist populations, or the common ancestral population could have been rainforest huntergatherers themselves! With respect to divergence among rainforest hunter-gatherer populations from different parts of Central Africa or among populations from different parts of Asia, we cannot be certain that the respective common ancestors of each group were full-time occupants of the rainforest. Specifically, there could have been multiple, independent transitions to full-time rainforest hunting and gathering within a continental region, as suggested by Bahuchet (1993) for Africa, and a hypothesis to which we will return in the next section of this paper. While analyses of genetic data from existing populations unfortunately cannot directly inform our understanding of where their genetic ancestors lived in the past (due to the possibility of population movement), it is at least possible to infer the dispersal rate of a current population over space by comparing patterns of genetic diversity with individual birthplace data (Rousset, 1997). Using this approach to study Baka rainforest hunter-gatherers from Cameroon, Verdu et al. (2010) estimated an average effective dispersal range of 12.4e63.2 km2. In the future, along with similar

Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038

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data from other populations, such approaches could potentially be further used to estimate the number of generations such a pattern must have existed in the same region in order to explain the overall pattern of genetic diversity, thus representing a lower-bound estimate for full-time rainforest occupation. An additional opportunity to address some of the uncertainty concerning the antiquity of full-time rainforest occupation could be a population genomics study of distinct groups who occupy adjacent regions of the same forest, such as the Efe and BaSua (very often also called BaMbuti) of the Ituri Forest in the DRC (Fig. 1). The Efe and BaSua share considerable phenotypic and cultural similarity but have adopted different languages (Sudanic and Bantu family languages, respectively) and have distinct hunting technologies e the Efe are generally archers and the BaSua are net hunters (Turnbull, 1965; Ichikawa, 1983; Hart and Hart, 1986; Roscoe, 1990). This cultural

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difference raises the possibility of a non-negligible population divergence time, which could be estimated pending DNA sample availability from participants of both groups. Due to the fact that it is more likely that a single ancestral population occupied the Ituri Forest and subsequently split, rather than for two distinct populations to have migrated separately to adjacent regions, the EfeeBaSua population divergence time would potentially serve as a lower bound estimate for the origin of full-time rainforest occupation by humans. 3. Ecological adaptations to the rainforest The incredible phenotype diversity observed among human populations worldwide is shaped by the combination of environmental effects on phenotypes, a history of genetic drift, and a history of natural selection. Technological and analytical advances in

Fig. 1. Approximate historical ranges of BaSua and Efe rainforest hunter-gatherers in the Ituri Forest. (A) BaSua (very often also called BaMbuti) man with net used for hunting, Democratic Republic of the Congo (DRC) (photograph by Nathaniel Dominy, with permission). (B) Efe man with bow, DRC (photograph by William Wheeler, with permission from the National Anthropological Archives, Smithsonian Institution [2005e19_sht19_094]). (C) Vegetation land cover map of the DRC, modified from Laporte et al. (1998). Remaining tropical forest areas (as of the early 1990s) are shown as dark green. Savanna domains are colored in browns. (D) The Ituri Forest region (including the Okapi Wildlife and Forestry Reserves) in Northeast DRC. Approximate territories of the BaSua (net hunters) and Efe (archers) rainforest hunter-gatherers (drawn from Turnbull, 1965) are shaded in blue and purple, respectively. The territory of a third rainforest hunter-gatherer group in the area, the Asua, is not shown. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038

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population genomics have facilitated a growing knowledge of local adaptation to specific environmental conditions in human populations (Tishkoff, 2015). Specifically, candidate signatures of recent positive natural selection in the genome can be identified, for example, by searching for genomic regions containing genetic variants with allele frequency differences between two or more populations that are unusually large compared to the remainder of the genome (Sabeti et al., 2006). Within a single population, methods to identify candidate signatures of recent positive selection include the identification of regions containing variants with allele frequencies that, compared to the genomic background, are higher than expected given their estimated age (Fu and Akey, 2013). Then, when these findings are evaluated against results from genotypeephenotype association studies (Bush and Moore, 2012), it is possible to make indirect inferences about the adaptive evolutionary history of a biological trait (Scheinfeldt and Tishkoff, 2013). Many of the evolutionary genomic studies of rainforest huntergatherers conducted to date have focused directly or indirectly on small body size, or the ‘pygmy’ phenotype. Based on the apparent convergent evolution of this trait in both African and Southeast populations (Perry and Dominy, 2009), human biologists have variably hypothesized that the pygmy phenotype is an adaptation to the particular ecological challenges of the tropical rainforest habitat, including to food limitation (Lopez Herraez et al., 2009), to thermoregulatory strains from high heat and humidity (CavalliSforza, 1986), to inefficient movement due to high structural forest density (Diamond, 1991), or indirectly to high adult mortality (Migliano et al., 2007). However, before considering whether the pygmy phenotype is an adaptation, or ecology-based hypotheses for its origin, it is important to confirm that the trait has a genetic basis (i.e., so that underlying variation thereof could have been affected by natural selection) rather than a purely environmental one as a function of food limitation or high parasitic pressures experienced during the growth period. Indeed, we now have strong evidence from multiple studies that the pygmy phenotype is explained to a substantial degree by genetic variation, as among the individuals within rainforest hunter-gatherer communities, stature is significantly positively correlated with the proportion of individual genomic ancestry from neighboring agriculturalist populations via their history of admixture (see next section) (Becker et al., 2011; Jarvis et al., 2012; Perry et al., 2014). To test whether the pygmy phenotype reflects a history of positive natural selection, population geneticists have used two general approaches. First, the population genomic methods described above have been used to scan the genome for signatures of recent (i.e., within the last ~30,000 years) positive selection, followed by comparison of the set of genes located within or nearest the detected signals to a database of known general biological functions for those genes (curated via studies conducted with other human populations and in non-human organisms; Ashburner et al., 2000). Multiple studies, considering both African and Southeast Asian rainforest hunter-gatherer populations, have used this approach to identify significant enrichments among genes located within the signatures of positive natural selection for those involved in growth, body development, the growth hormone pathway, and pituitary functions (Lopez Herraez et al., 2009; Jarvis et al., 2012; Lachance et al., 2012; Migliano et al., 2013; Amorim et al., 2015), a pattern at least not inconsistent with a history of natural selection on body size in these populations. For several genetic loci contained within regions of putative positive selection, follow-up analyses identified an association between genotype and stature phenotype (Jarvis et al., 2012; Lachance et al., 2012). In the most recently published study, Hsieh et al. (2016) used a genome-wide screen to identify multiple

strong candidate positive selection loci nearby genes involved in bone and muscle development in BiAka and Baka rainforest huntergatherers from the Central African Republic and Cameroon. In contrast, Perry et al. (2014) initially performed an admixturebased genome-wide association study in the BaTwa, a rainforest hunter-gatherer population from East Central Africa (Uganda), leading to the identification of 16 pygmy phenotype-associated genomic regions, followed by an analysis of the evolutionary histories of those regions. While the 16 regions were significantly enriched for genetic variants previously associated with adult stature in populations of European descent and for genes involved in growth hormone pathway functions, helping to validate their association with the pygmy phenotype, these regions were not enriched for the very strongest signatures of positive natural selection in the BaTwa genome (Perry et al., 2014). However, as a whole, the genetic variants within the BaTwa pygmy phenotype-associated genomic regions had slightly but significantly elevated selection statistic values and were also more differentiated between the BaTwa and their agricultural neighbors, the BaKiga, compared to the remainder of the genome (Perry et al., 2014). This observation is a signature of ‘polygenic’ adaptation (Pritchard and Di Rienzo, 2010; Pritchard et al., 2010; Turchin et al., 2012; Hsieh et al., 2016; Wellenreuther and Hansson, 2016), when natural selection acts on traits affected by multiple genetic variants across the genome, and phenotype evolution can be achieved by relatively subtle frequency changes of genetic variants in aggregate. Interestingly, in the same genomic regions associated with the BaTwa pygmy phenotype, similar signatures of polygenic adaptation were not observed in the Baka, a rainforest hunter-gatherer population from West Central Africa (Cameroon and Gabon). Although further study is needed, this result may suggest that the pygmy phenotype evolved convergently among different populations even within Africa (Perry et al., 2014). This notion is consistent with the finding from a recent analysis of longitudinal growth rates that rainforest hunter-gatherers from West vs. East Central Africa achieve small adult body size via distinct childhood growth patterns (Ramirez Rozzi et al., 2015). If correct, these results would suggest a relatively recent origin(s) of the African pygmy phenotype, evolving at least partially following the ~20,000 BP estimated divergence of West Central and East Central African rainforest hunter-gatherer populations (Patin et al., 2009). Scans for signatures of positive natural selection in rainforest hunter-gatherer populations also typically highlight genomic regions that do not contain genes involved in growth processes and stature (Lopez Herraez et al., 2009; Jarvis et al., 2012; Lachance et al., 2012; Migliano et al., 2013; Qian et al., 2013; Deng et al., 2014; Perry et al., 2014; Amorim et al., 2015; Hsieh et al., 2016). Such results are still of considerable interest, as they represent great opportunities for generating entirely new hypotheses about human adaptations to the challenging tropical rainforest habitat. For example, Lopez Herraez et al. (2009) hypothesized that signatures of positive natural selection near genes encoding proteins involved in the thyroid hormone pathway in African populations could reflect adaptations to a tropical rainforest environment deficient in iodine-rich foods. Other authors have investigated evolutionary signatures within sets of genes involved in processes such as thermoregulation, dietary metabolism, and reproductive maturation that could be related to particular ecological challenges of the tropical rainforest habitat for humans (Migliano et al., 2013; Amorim et al., 2015). 4. Rainforest hunter-gatherer interactions with agriculturalists The emergence of agriculture and its spread throughout tropical rainforest environments in Africa, Asia, and South America have

Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038

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been the subjects of numerous archaeological investigations (reviewed in Mazoyer and Roudart, 2006), but archaeological data have been limited in their ability to elucidate the consequences of this spread on the in situ hunter-gatherer populations with whom the agriculturalists came into contact. Furthermore, while the complex nature of current interactions between the now neighboring agriculturalist and rainforest hunter-gatherer populations in these regions have been widely studied from ethnological, sociological, linguistic, and economical perspectives (e.g., Meillassoux, 1981; Bahuchet, 1993; Hill and Hurtado, 1996; Joiris, 2003; Benjamin, 2013; Rupp, 2014; Takeushi, 2014), the prehistory of these relationships remain largely unknown. Population genomics provides a set of tools to both characterize existing relationships among rainforest hunter-gatherer and agricultural populations from a genetic (and hence reproductive) perspective, and to reconstruct the past demographic and admixture mechanisms that led to the genetic patterns observed today. Not only can these tools provide information about past events that affected populations as a whole, based on autosomal (i.e., chromosomes 1e22 of the nuclear genome) genetic variation, but they can further disentangle any differential female and male genetic contributions to the observed genetic landscape by comparing asymmetricallyinherited portions of the genome (i.e., mitochondrial DNA for female lineages, the non-recombining portion of the Y chromosome for male lineages, and the X chromosome that disproportionally reflects the population histories of males and females). Before our below discussion of results from specific studies on these topics, we would like to emphasize that all reports of the level of admixture and the timing of its occurrence in a particular population are estimates rather than absolute values, and analytical approaches may vary between studies. Thus, while observed patterns of variation in these results can be very useful for hypothesis generation, appropriate caution is also warranted. In nearly all studies conducted to date e in both Africa and Asia e analyses of genetic data have revealed evidence of at least some admixture between rainforest hunter-gatherers and their neighboring agriculturalist populations (e.g., Abdulla et al., 2009; Patin et al., 2009; Tishkoff et al., 2009; Verdu et al., 2009; Becker et al., 2011; Scholes et al., 2011; Jarvis et al., 2012; Migliano et al., 2013; Verdu et al., 2013; Deng et al., 2014; Patin et al., 2014; Perry et al., 2014; Hsieh et al., 2016). Observed patterns of admixture are typically highly asymmetrical at the population level, with gene flow primarily from the agriculturalist neighbors into the hunter-gatherer population and relatively little gene flow in the other direction. Admixture levels do vary widely among rainforest hunter-gatherer populations, for example in Africa from less than 10% (average per-individual agriculturalist ancestry) for the BaSua from the DRC to more than 50% for the Bongo from Gabon (Verdu et al., 2013; Patin et al., 2014; Hsieh et al., 2016). Similar variability exists in Asia, for example with admixture estimates for rainforest hunter-gatherer populations even only within the Philippines ranging from less than 10% for the Aeta to ~40% for the Agta and Batak (Abdulla et al., 2009; Migliano et al., 2013; Deng et al., 2014). Interestingly, at least in Africa, the agriculturalist genetic contribution to rainforest hunter-gatherer populations is consistently highly sex-biased, with gene flow primarily mediated via male rather than female agriculturalists (Destro-Bisol et al., 2004; Verdu et al., 2013). This male-biased introgression is also highly variable, ranging from a 3 to 1 ratio of male vs. female genetic introgression in the Bongo from Southeast Gabon to an extreme bias in the Koya from Gabon, for whom virtually complete replacement of the Y-chromosome from that of their neighboring agricultural population has been observed despite no trace of female-mediated gene flow (Verdu et al., 2013).

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In Central Africa, these patterns could be explained by a combination of inter-population socio-economic disparity and patrilocal post-marital practices (in which the bride moves to live with, or close to, the groom's family after marriage) that have been observed in the ethnographic record for numerous interacting agriculturalist and rainforest hunter-gatherer societies in this region (Kazadi, 1981; Bahuchet and Guillaume, 1982; Hewlett, 1996; Joiris, 2003; Takeushi, 2014). Specifically, agriculturalist females are often forbidden from marrying socio-economically discriminated-against hunter-gatherer males. While the reciprocal marriages e between agriculturalist males and hunter-gatherer females e are reported to happen more easily, this scenario should result in a population-level admixture pattern different than that observed, given patrilocality. However, such marriages very often end in a divorce, mainly due to social pressures endured by the discriminated hunter-gatherer female in her husband's community (Kazadi, 1981; Bahuchet and Guillaume, 1982; Hewlett, 1996; Joiris, 2003; Takeushi, 2014). Similar to the death of the husband, divorces also trigger the wife's return to the hunter-gatherer community, often with her admixed children. Interestingly, the absolute admixture levels are lower while the degrees of male-biased introgression are considerably higher in populations reporting stronger socio-economic discrimination (Destro-Bisol et al., 2004; Verdu et al., 2009, 2013; Patin et al., 2014). Finally, we have some developing insight from genomic methods into the timing of the onset of admixture between Central African hunter-gatherer and agriculturalists. In West Central Africa, admixture between agriculturalists and the BiAka and Baka may have occurred ~7000 BP (Hsieh et al., 2016). In East Central Africa, there is currently a discrepancy between two of the major analyses conducted to date. Gurdasani et al. (2015) estimate admixture between agriculturalists and Congo Basin hunter-gatherers at ~3000 BP, roughly concurrent with the arrival of agriculture into that region based on archaeological data (Eggert, 1993; Phillipson, 2005). In contrast, Patin et al. (2014) estimated an onset of admixture between African agriculturalist and various rainforest huntergatherer populations to within the past 1000 years BP, representing a substantial delay following the spread of agriculture into the rainforest regions where these populations live today. Recent linguistic- and paleoclimate-based models for the migration of Bantuspeaking agriculturalists into the Congo Basin rainforest could potentially help explain, at least in part, a delayed onset of genetic admixture. Specifically, the pace of migration and demographic expansion in this region may have been slowed by the difficulties of adapting agriculture to rainforest environments (Bostoen et al., 2015; Grollemund et al., 2015). We suspect that future analyses, benefitting from new methodological tools and whole genome sequence data (e.g., Hellenthal et al., 2014) will likely help to resolve the apparent discrepancies between the above studies and deliver increased precision to our understanding of the timing of the complex admixture events between tropical rainforest hunter-gatherer and agriculturalist populations, worldwide. 5. Conclusion As genomic technologies and methods continue to advance, we can likely look forward to additional major insights into human rainforest hunter-gatherer history and evolutionary ecology. For example, we expect that studies combining evolutionary genomic analyses with epigenomic (e.g., methylation) data (Fagny et al., 2015) or functional genomic (e.g., gene expression) data will help to further accelerate the pace of discovery and insight into the biological adaptations and ecological histories of human rainforest hunter-gatherer populations. In combination with those results,

Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038

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continued improvements in methods to estimate the timing of positive selection in the genome (e.g., Kelley, 2012; Chen and Slatkin, 2013; Fu et al., 2013; Sams et al., 2015) may help us understand better the paleoecological context of those adaptations. In addition, recent improvements in ancient DNA methods (Meyer et al., 2012; Dabney et al., 2013; Marciniak et al., 2015) offer hope for a future paleogenomics contribution to our understanding of human rainforest occupation history. While DNA preservation is poor in wet and warm environments, the list of successful tropical and subtropical ancient DNA studies has been growing (Letts and Shapiro, 2012; Gutierrez-Garcia et al., 2014; Brace et al., 2015; Gallego Llorente et al., 2015; Kistler et al., 2015; Schroeder et al., 2015). Moreover, while the recovery of ancient human remains from tropical forest habitats is challenged by the combination of preservation conditions and low population densities of mobile rainforest hunter-gatherers, human skeletal material has been recovered from several locations to date (Mercader et al., 2001; Barker et al., 2007; Perera et al., 2011; Roberts et al., 2015). If paleogenomic data are ultimately generated from prehistoric human tropical rainforest remains, it could then be possible to establish genetic continuity with the current hunter-gatherer inhabitants in the region. Doing so may not fully resolve questions of permanent vs. transient occupation (although an integrated analysis with stable isotope ratio data could potentially benefit this assessment; Roberts et al., 2015) but it would at least establish an antiquity of tropical rainforest habitat association, on at least a repeated basis, to help provide context for evolutionary ecology studies of the modern population descendants.

Acknowledgments We thank Patrick Roberts for inviting our contribution to this special issue, two reviewers for their comments that helped improve the manuscript, and Nate Dominy. Luis Barreiro, Serge de ric Austerlitz, Evelyne Heyer, Etienne Patin, LluisBahuchet, Fre Quintana-Murci, and Barry S. Hewlett for their ongoing collaboration and discussions with us on the topics presented in this review.

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Please cite this article in press as: Perry, G.H., Verdu, P., Genomic perspectives on the history and evolutionary ecology of tropical rainforest occupation by humans, Quaternary International (2016), http://dx.doi.org/10.1016/j.quaint.2016.04.038