Hybridization in human evolution: Insights from other organisms

Abstract

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex-differences in behavior, Haldane's rule and the large X-effect, and transgressive phenotypic variation.

Keywords: Neanderthals; gene flow; introgression; model organisms; modern human origins.

FIGURE 1

Illustration of the gradation from gene flow to introgression along a continuum of speciation, resulting in a reticulated pattern of speciation at the population level. Genetic distance refers to distance between the hybridizing parents (increasing as you move through time). Changing phenotypic effects with increasing genetic distance are shown to the right. Phenotypic variance refers to within population variance of the hybrid population. The shapes of the effect curves are qualitative and so not to any scale; though based on available evidence to date, they remain working hypotheses [Color figure can be viewed at wileyonlinelibrary.com]

FIGURE 2

Hypothesized directions and magnitudes of introgression in hominin evolution. Genetic evidence for known introgression indicated by black arrows between lineages. The green region indicates the time period of purported fossil (phenotypic) evidence for introgression between Neanderthals and H. sapiens (fossil/phenotypic evidence for introgression between Denisovans and other taxa is currently unknown, due to our limited understanding of the morphology of Denisovans). Genetic evidence of a first generation hybrid (Denisova 11) between Neanderthals and Denisovans is shown with a dotted line, though the introgressive effect of this on future lineages is currently unknown. Presumably, evidence (both genotypic and fossil/phenotypic) for gene flow earlier in the separation of lineages would be more difficult to detect, as would phenotypic/genotypic differences among the hybridizing taxa. This is consistent with the hominin fossil record of the middle Pleistocene [Color figure can be viewed at wileyonlinelibrary.com]

FIGURE 3

A comparison of facial variation among two Callithrix species and their hybrid. Left: Anthropogenic Callthrix penicillata x C. geoffroyi hybrid from Viçosa, MG, Brazil. Top right: C. geoffroyi. Bottom right: C. penicillata [Color figure can be viewed at wileyonlinelibrary.com]

FIGURE 4

Hybrid and purebred baboon crania, illustrating the wide variation and relatively large size of hybrids relative to their parent taxa. Top: Female baboons, with parent taxa on left (Papio anubis, top, P. cynocephalus, bottom), and three F1 hybrids on right. Bottom: male baboons, from left to right, F1 hybrid, F1 hybrid, P. cynocephalus, and P. anubis. Images reprinted from: Ackermann RR, Rogers J, and Cheverud JM. Identifying the morphological signatures of hybridization in primate and human evolution. J Hum Evol 51: 632–645, copyright (2006), with permission from Elsevier

FIGURE 5

Intermediate features of the Vindija Neandertals. Details and data are available in Smith, et al. clockwise from top left: (1) Vindija 259 left adult maxilla. Reconstructed nasal breadth falls almost three standard deviations (SDs) below the Neandertal mean. (2) Vindija mandible 206 (lingual view). An incipient incurvatio mandibulae and mentum osseum are visible on the external mandibular symphysis. (3) Vindija mandible 231, oriented to the alveolar plane. The almost vertical symphysis reflects reduction of facial prognathism. The symphyseal angles of vi 206 and vi 231 fall more than three SD below the Neandertal mean. (4) Vindija 231 mandible. The symphysis exhibits a weak outline of the mental trigone, a modern human feature [Color figure can be viewed at wileyonlinelibrary.com]