Why is Studying Ape Speciation Important?

The ape family, Hominidae, contains four extant genera: Pongo, consisting of the Sumatran and Bornean orangutans; Gorilla, consisting of western and eastern gorillas; Pan, consisting of common chimpanzees and bonobos; and finally Homo, consisting of humans (Figure 1). Of these, the African great apes, Pan and Gorilla, are our closest living relatives. A central focus of biological anthropology is to infer the evolutionary relationships that we share, to examine how our evolutionary history differs from apes, and, ultimately, to understand the unique adaptations that ‘make us human'. Many types of data have been used to answer these questions, including morphological, genetic, ecological and behavioral data. The late 20^th century saw an explosion of genetic studies that offered great insights into the shared evolutionary history of humans and apes. Such studies also raised questions about which evolutionary processes generated the diversity found in great ape species, and about how these processes differ across species. These studies also led to rich discussions about the suite of factors that may have contributed to promoting speciation in the last common ancestor of humans and African apes, as well as the factors that might have contributed to creating the amazing diversity of Hominins that co-existed with each other during the Pliocene and Pleistocene (Foley 2002).

How are We Related to African Apes?

For many years, there was considerable debate about which of the African apes is our closest relative. The general consensus that emerged is that we share a more recent relationship with chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) than we do with gorillas (Gorilla gorilla) (Ruvolo 1997, Chen & Li 2001). This consensus was bolstered by initial comparisons of the chimpanzee and human genomes (Consortium 2005). Chimpanzees and bonobos share 99% of their genomes with humans in regions of their genomes that can be directly aligned and compared. Gorillas are a close second, sharing 98%, and orangutans come in third, sharing 97% of their genome with us. The lineage ultimately leading to modern humans separated from the lineages leading to chimpanzees and bonobos 5.5–7 million years ago (mya), from the lineage leading to gorillas 8.5–12 mya, and from the lineages leading to orangutans 9–13 mya.

Detailed comparisons between the complete genomes of each species have recently been completed. These studies suggest that the speciation process leading to the separation of the human-chimpanzee/bonobo-gorilla ancestor was quite complex, and that the separation of these lineages occurred so closely in time that they are difficult to disentangle. In particular, the genealogical relationships between humans and African apes vary across the genome. For instance, comparing the gorilla genome to those of human and chimpanzee suggested that across about 15% of their genome, gorillas share a closer relationship with humans than they do with chimpanzees (Scally et al. 2012). Chimpanzees and bonobos last shared a common ancestor with each other about 1–1.5 mya. As expected then, the genomes of bonobo and chimpanzee are mostly equally distant from human. However, across about 3% of the human genome this relationship is unequal, where humans are closer to bonobos than they are to chimpanzees, while in others, humans are closer to chimpanzees (Prufer et al. 2012). Making the entire picture more complex is the fact that this variation in evolutionary relationships is not just limited to comparisons of African apes to humans. Across about 0.8% of our genome, humans are also more closely related to orangutans than to chimpanzees (Hobolth et al. 2011, Locke et al. 2011).

What can explain these conflicting findings? Speciation occurs in populations that have genetic diversity. This fact is important because this diversity can result in gene trees and species trees that do not always match (Figure 2), sometimes as a result of incomplete lineage sorting (ILS) (Hobolth et al. 2011). ILS can be the result of many factors, including the degree of genetic diversity at a given locus in an ancestral population; whether the rate of divergence at a particular locus is equal or unequal to the rate at which speciation occurred; and gene loss and gene duplication events. Other factors can also lead to gene-tree and species-tree incongruence, including hybridization between descendant species; differences in recombination across the genome; and the action of natural selection during and after the separation of an ancestor into its descendants (Degnan & Rosenberg 2009). Each scenario can be supported by genome comparisons. For instance, Patterson et al. (2006) found dramatically reduced ILS along the X-chromosome, as well as lower genetic diversity, in human and chimpanzee compared to gorilla. Using this evidence, they proposed that hybridization occurred between the ancestors of the chimpanzee and human lineages after their initial separation from each other (Patterson et al. 2006), although this conclusion is debated (Presgraves & Yi 2009). In addition, comparisons of differences in gene expression profiles have shown significant overlap in regions of the genome that appear to be subject to ILS in human, chimpanzee, and gorilla (Scally et al. 2012), demonstrating that this phenomenon can be reflected in functional differences between species.

How do the Evolutionary Histories of Humans and African Apes Differ, and What Properties do They Share?

Since speciation begins in populations, understanding it requires comparing the processes that generate evolutionary diversification within and between populations, and how these processes vary between species. Speciation and population differentiation can occur through either neutral evolutionary processes, such as genetic drift, by natural selection that results in local adaptation of different populations, or through a combination of both (Safran & Nosil 2012). Each process generates genetic diversity, but they are difficult to tease apart from one another (Coop et al. 2009). Consider, for example, the history of our species. Genetic, archeological, and fossil data suggest that modern humans first appeared in Africa then migrated elsewhere (Campbell & Tishkoff 2010). This history is reflected in our gene pool, especially at genetic loci that evolve neutrally. Africans are the most diverse populations, and non-Africans have a subset of the genetic diversity found in Africans. Our species also has a small effective population size, consistent with a small number of Africans exiting the continent and populating the rest of the world. This history also included co-opting some of the genomes of Neanderthals and Denisovans (Green et al. 2010, Reich et al. 2010) whose ancestors migrated out of Africa earlier. This demographic history, however, is also superimposed over another layer of history that includes local adaptation of different populations to a number of variables (Sabeti et al. 2006), most notably, adaptations to different pathogens (Omenn 2010, Fumagalli et al. 2011), such as malaria (Kwiatkowski 2005). The post-genome era has greatly improved studies that focus on disentangling demographic history from more subtle selective pressures, such as differences in lifestyles. As a result, a variety of other factors are also recognized as important drivers of local adaptation in our species, such as differences in milk (Tishkoff et al. 2007) and carbohydrate consumption (Hancock et al. 2010). In contrast to humans, little is known about the mechanisms that underlie the diversification of African apes. Yet, examining these mechanisms is critical for understanding how different factors influence processes that generate diversity in apes vs. humans.

African apes are a diverse group that occupy a number of different habitats (Caldecott et al. 2005). Gorillas are found in lowland rainforest and montane forests across equatorial Africa and are divided into two species, with each one further partitioned into two additional subspecies (Figure 3). Bonobos belong to a single species located in the rainforests south of the Congo River. In contrast, chimpanzees have the widest geographic distribution, and are found north of the Congo in a range of habitats, including lowland rainforest, savannas, and forest-savanna mosaics. Chimpanzees show considerable genetic diversity across their range, and are divided into four subspecies (Gonder et al. 2011, Bowden et al. 2012). The genetic and demographic histories of African apes are remarkably different from the history of modern humans. Compared to humans, the various regional populations, or subspecies, of apes generally share more distant last common ancestors with each other, have historically had larger effective population sizes, and exchange fewer migrants between populations (Stone & Verrelli 2006).

There are still mysteries regarding the processes that have generated this diversity in African apes. On the one hand, the patterning of African ape genetic diversity is thought to have been driven, at least in part, by neutral evolutionary processes (e.g., drift, gene flow, population expansions) that are associated with the historic contraction and expansion of forests into ‘Pleistocene Refugia' (Anthony et al. 2007). Similarly, the separation of ape species and subspecies across riverine boundaries, like the Congo and Sanaga Rivers, likely played an important role in generating their current pattern of evolutionary diversification (Gonder et al. 2011, Bowden et al. 2012) . On the other hand, little is known about how local adaptation contributed to generating patterns of genetic diversity found among African apes, but natural selection was probably very important. Similar to humans, signatures of local adaptation in African apes are likely to be superimposed on the demographic history of the species.

A range of factors might contribute to local adaptation in apes, including pathogens, habitat variation, and differences in diet, among others. Chimpanzees, for example, show population-specific signatures of selection at genes important in immune response (MacFie et al. 2009, de Groot et al. 2010), suggesting that local adaptations in host defenses have been important in shaping patterns of genetic variation in this species. Habitat variation may also contribute to local adaptation among apes. For instance, across the broad spectrum of habitats where chimpanzees are found, communities living in rainforests and savannas exhibit differences in their behavior, diet, and ranging patterns (Stumpf 2007). It has long been proposed that this variation in their socioecology might be evidence of local adaptation to different ecological niches (Moore 1996). What is unknown is whether such local ‘adaptations' are correlated with genetic differentiation, which is a necessary precursor to speciation. Future studies that incorporate ecological, behavioral, and genetic data hold great potential to expand knowledge about how neutral evolutionary processes and local adaptation have differentially contributed to generating the remarkable diversity found among the African apes.

Summary

Complete human, chimpanzee, bonobo, gorilla, and orangutan genomes have provided us a window into understanding the complex speciation process of these species' common ancestor. Analyses of these genomes overwhelmingly support the hypothesis that chimpanzees are our closest relatives, but speciation occurred over such a brief period of time that it left our genome a mosaic of shared ancestry with each of the extant apes. The processes that generated this pattern were complex, and may be explained by a combination of both neutral evolutionary processes, as well as natural selection leading to local adaptation. It is unclear how they may have differentially contributed to generating this genetic pattern, or how each process might be superimposed upon one another. A clearer understanding about how neutral processes and local adaptation have influenced the genetic history of each species is vital for inferring how such processes contributed to the speciation of the last common ancestor of African apes and humans. Such studies will explain what properties of the speciation process were shared between apes and Hominins, how they differed, and ultimately, provide clues about what ‘makes us human'.