Hans R. Siegismund

Great ape genetic diversity and population history

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

The Confounding Effect of Population Structure on Bayesian Skyline Plot Inferences of Demographic History

Many coalescent-based methods aiming to infer the demographic history of populations assume a single, isolated and panmictic population (i.e. a Wright-Fisher model). While this assumption may be reasonable under many conditions, several recent studies have shown that the results can be misleading when it is violated. Among the most widely applied demographic inference methods are Bayesian skyline plots (BSPs), which are used across a range of biological fields. Violations of the panmixia assumption are to be expected in many biological systems, but the consequences for skyline plot inferences have so far not been addressed and quantified. We simulated DNA sequence data under a variety of scenarios involving structured populations with variable levels of gene flow and analysed them using BSPs as implemented in the software package BEAST. Results revealed that BSPs can show false signals of population decline under biologically plausible combinations of population structure and sampling strategy, suggesting that the interpretation of several previous studies may need to be re-evaluated. We found that a balanced sampling strategy whereby samples are distributed on several populations provides the best scheme for inferring demographic change over a typical time scale. Analyses of data from a structured African buffalo population demonstrate how BSP results can be strengthened by simulations. We recommend that sample selection should be carefully considered in relation to population structure previous to BSP analyses, and that alternative scenarios should be evaluated when interpreting signals of population size change.

Comparative phylogeography of African savannah ungulates

The savannah biome of sub‐Saharan Africa harbours the highest diversity of ungulates (hoofed mammals) on Earth. In this review, we compile population genetic data from 19 codistributed ungulate taxa of the savannah biome and find striking concordance in the phylogeographic structuring of species. Data from across taxa reveal distinct regional lineages, which reflect the survival and divergence of populations in isolated savannah refugia during the climatic oscillations of the Pleistocene. Data from taxa across trophic levels suggest distinct savannah refugia were present in West, East, Southern and South‐West Africa. Furthermore, differing Pleistocene evolutionary biogeographic scenarios are proposed for East and Southern Africa, supported by palaeoclimatic data and the fossil record. Environmental instability in East Africa facilitated several spatial and temporal refugia and is reflected in the high inter‐ and intraspecific diversity of the region. In contrast, phylogeographic data suggest a stable, long‐standing savannah refuge in the south.

Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population

We investigated introgression in a mixed weedy population ofoilseed rape (Brassica napus) and itsrelative B. rapa usingspecies-specific AFLP-markers. The population wassituated in a field relayed from conventional to organic cultivation11 years ago. One-hundred-and-twoB. napus orB. rapa-like plantswere collected in a 3 m2 plot. Of these, onewas a first generation hybrid (F1) and nearlyhalf (44 plants) were introgressed, having bothB. napus andB. rapa specific markers.The remaining plants apparently corresponded to pure species, with 50having only B. rapa-and seven having only B.napus-specific markers. We compared thenumber of markers in the plants from the weedy population with thenumbers in controlled backcross generations (BC1 andBC2). The marker distribution in the weedy populationresembled the distribution in the second backcross generation mostclosely. Together with the cultivation history of the field, thissuggests that the introgression process in the weedy mixed populationhas been in progress for some time. This study is the first to showintrogression between B.napus and B.rapa under natural conditions.

Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci : High variation but low differentiation

The African buffalo (Syncerus caffer) is widespread throughout sub‐Saharan Africa and is found in most major vegetation types, wherever permanent sources of water are available, making it physically able to disperse through a wide range of habitats. Despite this, the buffalo has been assumed to be strongly philopatric and to form large aggregations that remain within separate home ranges with little interchange between units, but the level of differentiation within the species is unknown. Genetic differences between populations were assessed using mitochondrial DNA (control region) sequence data and analysis of variation at six microsatellite loci among 11 localities in eastern and southern Africa. High levels of genetic variability were found, suggesting that reported severe population bottlenecks due to outbreak of rinderpest during the last century did not strongly reduce the genetic variability within the species. The high level of genetic variation within the species was found to be evenly distributed among populations and only at the continental level were we able to consistently detect significant differentiation, contrasting with the assumed philopatric behaviour of the buffalo. Results of mtDNA and microsatellite data were found to be congruent, disagreeing with the alleged male‐biased dispersal. We propose that the observed pattern of the distribution of genetic variation between buffalo populations at the regional level can be caused by fragmentation of a previous panmictic population due to human activity, and at the continental level, reflects an effect of geographical distance between populations.

Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding

Genomes in the mist The mountain gorilla is an iconic species that is at high risk of extinction. Xue et al. have sequenced 13 gorillas from two different populations to probe their genetic diversity. The genomes show large tracts of homozygosity and the loss of highly deleterious genetic variants, indicating population bottlenecks and inbreeding. This loss of genetic diversity appears to have started over 20,000 years ago and may have been caused by changes in climate and human-associated effects. Science, this issue p. 242 Inbreeding in mountain gorillas increases the threat from disease and environmental change but has purged deleterious mutations. Mountain gorillas are an endangered great ape subspecies and a prominent focus for conservation, yet we know little about their genomic diversity and evolutionary past. We sequenced whole genomes from multiple wild individuals and compared the genomes of all four Gorilla subspecies. We found that the two eastern subspecies have experienced a prolonged population decline over the past 100,000 years, resulting in very low genetic diversity and an increased overall burden of deleterious variation. A further recent decline in the mountain gorilla population has led to extensive inbreeding, such that individuals are typically homozygous at 34% of their sequence, leading to the purging of severely deleterious recessive mutations from the population. We discuss the causes of their decline and the consequences for their future survival.

Population structure of the African savannah elephant inferred from mitochondrial control region sequences and nuclear microsatellite loci

Two hundred and thirty-six mitochondrial DNA nucleotide sequences were used in combination with polymorphism at four nuclear microsatellite loci to assess the amount and distribution of genetic variation within and between African savannah elephants. They were sampled from 11 localities in eastern, western and southern Africa. In the total sample, 43 haplotypes were identified and an overall nucleotide diversity of 2.0% was observed. High levels of polymorphism were also observed at the microsatellite loci both at the level of number of alleles and gene diversity. Nine to 14 alleles per locus across populations and 44 alleles in the total sample were found. The gene diversity ranged from 0.51 to 0.72 in the localities studied. An analysis of molecular variance showed significant genetic differentiation between populations within regions and also between regions. The extent of subdivision between populations at the mtDNA control region was approximately twice as high as shown by the microsatellite loci (mtDNA FST = 0.59; microsatellite RST = 0.31). We discuss our results in the light of Pleistocene refugia and attribute the observed pattern to population divergence in allopatry accompanied by a recent population admixture following a recent population expansion.

Extensive X-linked adaptive evolution in central chimpanzees

Surveying genome-wide coding variation within and among species gives unprecedented power to study the genetics of adaptation, in particular the proportion of amino acid substitutions fixed by positive selection. Additionally, contrasting the autosomes and the X chromosome holds information on the dominance of beneficial (adaptive) and deleterious mutations. Here we capture and sequence the complete exomes of 12 chimpanzees and present the largest set of protein-coding polymorphism to date. We report extensive adaptive evolution specifically targeting the X chromosome of chimpanzees with as much as 30% of all amino acid replacements being adaptive. Adaptive evolution is barely detectable on the autosomes except for a few striking cases of recent selective sweeps associated with immunity gene clusters. We also find much stronger purifying selection than observed in humans, and in contrast to humans, we find that purifying selection is stronger on the X chromosome than on the autosomes in chimpanzees. We therefore conclude that most adaptive mutations are recessive. We also document dramatically reduced synonymous diversity in the chimpanzee X chromosome relative to autosomes and stronger purifying selection than for the human X chromosome. If similar processes were operating in the human–chimpanzee ancestor as in central chimpanzees today, our results therefore provide an explanation for the much-discussed reduction in the human–chimpanzee divergence at the X chromosome.

Extreme genetic differences among populations of Gazella granti, Grant's gazelle, in Kenya

Mitochondrial DNA (mtDNA) control region sequences from six Kenyan Grants gazelle (Gazella granti) populations were highly divergent among locations. Neighbouring populations not separated by geographical or vegetational barriers exhibited a nucleotide sequence divergence of about 14 per cent. A similar level of divergence separates Grants gazelles from a closely related species, the Soemmerings gazelle (G. soemmeringii). Nuclear microsatellite repeat number variation at two loci also indicated substantial population genetic differentiation. Despite high levels of sequence divergence, populations of Grants gazelles were more closely related to each other than to Soemmerings and Thomsons gazelles (G. thomsoni) as measured by nucleotide sequence divergence at the mtDNA protein coding cytochrome b gene and the nuclear α-lactalbumin gene. This pattern of extensive differentiation is hypothesized to have resulted from recently established contacts between formerly allopatric populations.

Phylogeography and population structure of the common warthog (Phacochoerus africanus) inferred from variation in mitochondrial DNA sequences and microsatellite loci.

Global climate fluctuated considerably throughout the Pliocene and Pleistocene, influencing the evolutionary history of a wide range of species. Using both mitochondrial sequences and microsatellites, we have investigated the evolutionary consequences of such environmental fluctuation for the patterns of genetic variation in the common warthog, sampled from 24 localities in Africa. In the sample of 181 individuals, 70 mitochondrial DNA haplotypes were identified and an overall nucleotide diversity of 4.0% was observed. The haplotypes cluster in three well-differentiated clades (estimated net sequence divergence of 3.1–6.6%) corresponding to the geographical origins of individuals (i.e. eastern, western and southern African clades). At the microsatellite loci, high polymorphism was observed both in the number of alleles per locus (6–21), and in the gene diversity (in each population 0.59–0.80). Analysis of population differentiation indicates greater subdivision at the mitochondrial loci (FST=0.85) than at nuclear loci (FST=0.20), but both mitochondrial and nuclear loci support the existence of the three warthog lineages. We interpret our results in terms of the large-scale climatic fluctuations of the Pleistocene.