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Evidence for Late Pleistocene origin of Astyanax mexicanus cavefish

View ORCID ProfileJulien Fumey, View ORCID ProfileHélène Hinaux, Céline Noirot, Claude Thermes, Sylvie Rétaux, View ORCID ProfileDidier Casane
doi: https://doi.org/10.1101/094748
Julien Fumey
1Évolution, Génomes, Comportement, Écologie. CNRS, IRD, Univ Paris-Sud. Université Paris-Saclay. F-91198 Gif-sur-Yvette, France.
2Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, UMR 9198, FRC 3115, Avenue de la Terrasse, Bâtiment 24, Gif-sur-Yvette, Paris F-91198, France.
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Hélène Hinaux
3DECA group, Paris-Saclay Institute of Neuroscience, UMR 9197, CNRS, Gif sur Yvette, France.
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Céline Noirot
4Plateforme Bioinformatique Toulouse, Midi-Pyrénées, UBIA, INRA, Auzeville Castanet-Tolosan, France
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Claude Thermes
2Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, UMR 9198, FRC 3115, Avenue de la Terrasse, Bâtiment 24, Gif-sur-Yvette, Paris F-91198, France.
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Sylvie Rétaux
3DECA group, Paris-Saclay Institute of Neuroscience, UMR 9197, CNRS, Gif sur Yvette, France.
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Didier Casane
1Évolution, Génomes, Comportement, Écologie. CNRS, IRD, Univ Paris-Sud. Université Paris-Saclay. F-91198 Gif-sur-Yvette, France.
5Université Paris Diderot, Sorbonne Paris Cité, France.
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  • For correspondence: Didier.Casane@egce.cnrs-gif.fr
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Abstract

Background Cavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They share similar phenotypic changes such as blindness and depigmentation resulting from independent and convergent evolution. As such they allow examining whether their evolution involved the fixation of preexisting standing genetic variations and/or de novo mutations. Cavefish populations are currently assigned to two main groups, the so-called "old" and "new" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations.

Results First, we reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages, neither the ancient origin of the “old” lineage. Using IMa2, a program based on a method that does not assume that populations are at mutation/migration/drift equilibrium and thus allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (i.e. less than 20,000 years). Second, we identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to the “old” Pachón cave population and a surface population from Texas. Pachón cave population has accumulated more neutral substitutions than the surface population and we showed that it could be another signature of its recent origin. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years.

Conclusions Although it is often assumed that some cave populations such as Pachón cavefish have a very ancient origin, within the range of the late Miocene to the middle Pleistocene, a recent origin of these populations is strongly supported by our analyses of two independent sets of nuclear DNA polymorphism using two very different methods of analysis. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted October 27, 2017.
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Evidence for Late Pleistocene origin of Astyanax mexicanus cavefish
Julien Fumey, Hélène Hinaux, Céline Noirot, Claude Thermes, Sylvie Rétaux, Didier Casane
bioRxiv 094748; doi: https://doi.org/10.1101/094748
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Evidence for Late Pleistocene origin of Astyanax mexicanus cavefish
Julien Fumey, Hélène Hinaux, Céline Noirot, Claude Thermes, Sylvie Rétaux, Didier Casane
bioRxiv 094748; doi: https://doi.org/10.1101/094748

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