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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

ABSTRACT: How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.

SUBMITTER: Ma T

PROVIDER: S-EPMC5777044 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

Ma Tao T Wang Kun K Hu Quanjun Q Xi Zhenxiang Z Wan Dongshi D Wang Qian Q Feng Jianju J Jiang Dechun D Ahani Hamid H Abbott Richard J RJ Lascoux Martin M Nevo Eviatar E Liu Jianquan J

Proceedings of the National Academy of Sciences of the United States of America 20171226 2

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-r ...[more]

PMID: 29279400

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Project description:BackgroundThe processes leading to the diversity of over 7000 present-day languages have been the subject of scholarly interest for centuries. Several factors have been suggested to contribute to the spatial segregation of speaker populations and the subsequent linguistic divergence. However, their formal testing and the quantification of their relative roles is still missing. We focussed here on the early stages of the linguistic divergence process, that is, the divergence of dialects, with a special focus on the ecological settings of the speaker populations. We adopted conceptual and statistical approaches from biological microevolution and parallelled intra-lingual variation with genetic variation within a species. We modelled the roles of geographical distance, differences in environmental and cultural conditions and in administrative history on linguistic divergence at two different levels: between municipal dialects (cf. in biology, between individuals) and between dialect groups (cf. in biology, between populations).ResultsWe found that geographical distance and administrative history were important in separating municipal dialects. However, environmental and cultural differences contributed markedly to the divergence of dialect groups. In biology, increase in genetic differences between populations together with environmental differences may suggest genetic differentiation of populations through adaptation to the local environment. However, our interpretation of this result is not that language itself adapts to the environment. Instead, it is based on Homo sapiens being affected by its environment, and its capability to adapt culturally to various environmental conditions. The differences in cultural adaptations arising from environmental heterogeneity could have acted as nonphysical barriers and limited the contacts and communication between groups. As a result, linguistic differentiation may emerge over time in those speaker populations which are, at least partially, separated.ConclusionsGiven that the dialects of isolated speaker populations may eventually evolve into different languages, our result suggests that cultural adaptation to local environment and the associated isolation of speaker populations have contributed to the emergence of the global patterns of linguistic diversity.

Dataset Information

Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

Publications

Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

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