Goudet, J. — Page 2 | bioRxiv Science

bioRxiv2021

Genomic consequences of colonisation, migration and genetic drift in barn owl insular populations of the eastern Mediterranean

The study of insular populations was key in the development of evolutionary theory. The successful colonisation of an island depends on the geographic context, and specific characteristics of the organism and the island, but also on stochastic processes. As a result, apparently identical islands may harbour populations with contrasting histories. Here, we use whole genome sequences of 65 barn owls to investigate the patterns of inbreeding and genetic diversity of insular populations in the eastern Mediterranean Sea. We focus on Crete and Cyprus, islands with similar size, climate and distance to mainland, that provide natural replicates for a comparative analysis of the impacts of microevolutionary processes on isolated populations. We show that barn owl populations from each island have a separate origin, Crete being genetically more similar to other Greek islands and mainland Greece, and Cyprus more similar to the Levant. Further, our data show that their respective demographic histories following colonisation were also distinct. On the one hand, Crete harbours a small population and maintains very low levels of gene flow with neighbouring populations. This has resulted in low genetic diversity, strong genetic drift, increased relatedness in the population and remote inbreeding. Cyprus, on the other hand, appears to maintain enough gene flow with the mainland to avoid such an outcome. Our work provides a comparative population genomic analysis of the effects of neutral processes on a classical island-mainland model system. It provides empirical evidence for the role of stochastic processes in determining the fate of diverging isolated populations.

evolutionary biology↗

bioRxiv2021

Landscape and climatic variations of the Quaternary shaped multiple secondary contacts among barn owls (Tyto alba) of the Western Palearctic

The combined actions of climatic variations and landscape barriers shape the history of natural populations. When organisms follow their shifting niches, obstacles in the landscape can lead to the splitting of populations, on which evolution will then act independently. When two such populations are reunited, secondary contact occurs in a broad range of admixture patterns, from narrow hybrid zones to the complete dissolution of lineages. A previous study suggested that barn owls colonized the Western Palearctic after the last glaciation in a ring-like fashion around the Mediterranean Sea, and conjectured an admixture zone in the Balkans. Here, we take advantage of whole-genome sequences of 94 individuals across the Western Palearctic to reveal the complex history of the species in the region using observational and modeling approaches. Even though our results confirm that two distinct lineages colonized the region, one in Europe and one in the Levant, they suggest that it predates the last glaciation and identify a narrow secondary contact zone between the two in Anatolia. Nonetheless, we also show that barn owls re-colonized Europe after the glaciation from two distinct glacial refugia: a western one in Iberia and an eastern one in Italy. Both glacial lineages now communicate via eastern Europe, in a wide and permeable contact zone. This complex history of populations enlightens the taxonomy of Tyto alba in the region, highlights the key role played by mountain ranges and large water bodies as barriers and illustrates the power of population genomics in uncovering intricate demographic patterns.

evolutionary biology↗

bioRxiv2021

Unexpected post-glacial colonisation route explains the white colour of barn owls (Tyto alba) from the British Isles

The climate fluctuations of the Quaternary shaped the movement of species in and out of glacial refugia. In Europe, the majority of species followed one of the described traditional postglacial recolonization routes from the southern peninsulas towards the north. Like most organisms, barn owls are assumed to have colonized the British Isles by crossing over Doggerland, a land bridge that connected Britain to northern Europe. However, while they are dark rufous in northern Europe, barn owls in the British Isles are conspicuously white, a contrast that could suggest selective forces are at play on the islands. However, analysis of known candidate genes involved in colouration found no signature of selection. Instead, using whole genome sequences and species distribution modelling, we found that owls colonised the British Isles soon after the last glaciation, directly from a white coloured refugium in the Iberian Peninsula, before colonising northern Europe. They would have followed a yet unknown post-glacial colonization route to the Isles over a westwards path of suitable habitat in now submerged land in the Bay of Biscay, thus not crossing Doggerland. As such, they inherited the white colour of their Iberian founders and maintained it through low gene flow with the mainland that prevents the import of rufous alleles. Thus, we contend that neutral processes likely explain this contrasting white colour compared to continental owls. With the barn owl being a top predator, we expect future research will show this unanticipated route was used by other species from its paleo community.

evolutionary biology↗

bioRxiv2018

Assessing natural selection during range expansions: Insights from a spatially explicit ABC study

For at least 40 years now, evolutionary biologists have discussed the relative roles of natural selection and genetic drift in shaping the genetic composition of populations. Range expansions are of particular interest in this discussion: They normally occur over environmental gradients allowing local adaptation to take place, but the demographic properties of these expansions also potentiate genetic-drift effects, which may in turn randomly generate extreme changes in allele frequencies as populations expand in territory and numbers (i.e. allele surfing). Here, we address the detection and measurement of selection in such scenario using simulations. We mimic a range expansion over a variable selective gradient where individuals have in their genomes both loci that are neutral and loci determining a quantitative trait subject to selection. The responsiveness of summary statistics to the selective pressure is then assessed, and estimates of the selective pressure are made - based on these statistics - with approximate Bayesian computation (ABC). We observe that statistics related to isolation-by-distance patterns present a strong response to selection. This response can be used in ABC to estimate the strength of selection acting on the simulated populations with very reliable measures of estimability, regardless of the genetic architecture underlying the selected trait. Furthermore, these estimates are robust to noise produced by other genetic and demographic parameters such as heritability, mutation, migration and population-growth rates. This approach of taking into account the spatial dimension of differentiation in quantitative traits offers a promising avenue of investigation about the role of natural selection in range-expansion scenarios, with possible implementations in the study of natural cases, as well.

evolutionary biology↗

bioRxiv2017

Population Differentiation at the HLA Genes

Balancing selection is defined as a class of selective regimes that maintain polymorphism above what is expected under neutrality. Theory predicts that balancing selection reduces population differentiation, as measured by FST. However, balancing selection regimes in which different sets of alleles are maintained in different populations could increase population differentiation. To tackle this issue, we investigated population differentiation at the HLA genes, which constitute the most striking example of balancing selection in humans. We found that population differentiation of single nucleotide polymorphisms (SNPs) at the HLA genes is on average lower than that of SNPs in other genomic regions. However, this result depends on accounting for the differences in allele frequency between selected and putatively neutral sites. Our finding of reduced differentiation at SNPs within HLA genes suggests a predominant role of shared selective pressures among populations at a global scale. However, in pairs of closely related populations, where genome-wide differentiation is low, differentiation at HLA is higher than in other genomic regions. This pattern was reproduced in simulations of overdominant selection. We conclude that population differentiation at the HLA genes is generally lower than genome-wide, but it may be higher for recently diverged population pairs, and that this pattern can be explained by a simple overdominance regime.

genetics↗

bioRxiv2017

Complex genetic patterns in human arise from a simple range-expansion model over continental landmasses

Although it is generally accepted that geography is a major factor shaping human genetic differentiation, it is still disputed how much of this differentiation is a result of a simple process of isolation-by-distance, and if there are factors generating distinct clusters of genetic similarity. We address this question using a geographically explicit simulation framework coupled with an Approximate Bayesian Computation approach. Based on six simple summary statistics only, we estimated the most probable demographic parameters that shaped modern human evolution under an isolation by distance scenario, and found these were the following: an initial population in East Africa spread and grew from 4000 individuals to 5.7 million in about 132 000 years. Subsequent simulations with these estimates followed by cluster analyses produced results nearly identical to those obtained in real data. Thus, a simple diffusion model from East Africa explains a large portion of the genetic diversity patterns observed in modern humans. We argue that a model of isolation by distance along the continental landmasses might be the relevant null model to use when investigating selective effects in humans and probably many other species.

genetics↗

bioRxiv2016

A unified characterization of population structure and relatedness.

Many population genetic activities, ranging from evolutionary studies to association mapping to forensic identification, rely on appropriate estimates of population structure or relatedness. All applications require recognition that quantities with an underlying meaning of allelic identity by descent are not defined in an absolute sense, but instead are made \"relative to\" some set of alleles other than the target set. The early Weir and Cockerham FST estimate made explicit that the reference set of alleles was across independent populations. Standard kinship estimates have an implicit assumption that pairs of individuals in a study sample, other than the target pair, are unrelated, whereas other estimates assume alleles within individuals are not identical by descent. However, populations lose independence when there is migration between them, and when individuals in a study are related it is difficult to see how they can also be non-inbred. We have therefore re-cast our treatments of population structure, relatedness and inbreeding to make explicit that the parameters of interest involve differences of probabilities of identity by descent in the target and the reference sets of alleles and so can be negative. We take the reference set to be for the population from which study individuals have been sampled. We provide simple moment estimates of these parameters, phrased in terms of allele matching within and between individuals for relatedness and inbreeding, or within and between populations for population structure. A multi-level hierarchy of alleles within individuals, alleles between individuals within populations, and alleles between populations allows a unified treatment of relatedness and population structure. Our new estimates appear to be sensitive to rare or private variants, to give indications of the effects of natural selection, and to be appropriate for use in association studies.

genetics↗

bioRxiv2016

A Unified Characterization ofPopulation Structure and Relatedness

Many population genetic activities, ranging from evolutionary studies to association mapping to forensic identification, rely on appropriate estimates of population structure or relatedness. All applications require recognition that quantities with an underlying meaning of allelic identity by descent are not defined in an absolute sense, but instead are made \"relative to\" some set of alleles other than the target set. The early Weir and Cockerham FST estimate made explicit that the reference set of alleles was across independent populations. Standard kinship estimates have an implicit assumption that pairs of individuals in a study sample, other than the target pair, are unrelated, whereas other estimates assume alleles within individuals are not identical by descent. However, populations lose independence when there is migration between them, and when individuals in a study are related it is difficult to see how they can also be non-inbred. We have therefore re-cast our treatments of population structure, relatedness and inbreeding to make explicit that the parameters of interest involve differences of probabilities of identity by descent in the target and the reference sets of alleles and so can be negative. We take the reference set to be for the population from which study individuals have been sampled. We provide simple moment estimates of these parameters, phrased in terms of allele matching within and between individuals for relatedness and inbreeding, or within and between populations for population structure. A multi-level hierarchy of alleles within individuals, alleles between individuals within populations, and alleles between populations allows a unified treatment of relatedness and population structure. Our new estimates appear to be sensitive to rare or private variants, to give indications of the effects of natural selection, and to be appropriate for use in association studies.

genetics↗