Genomic signatures associated with transitions to viviparity in Cyprinodontiformes

Yusuf, Leeban; Lemus, Yolitzi Saldívar; Thorpe, Peter; Garcı́a, Constantino Macı́as; Ritchie, Michael G.

doi:10.1101/2022.05.25.493474

Cited by 3 publications

(3 citation statements)

References 128 publications

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“…We also found evidence of introgression of genes involved in adaptive immune response between A. toweri and an ancestral lineage leading to the divergence of Ameca, Xenoophorus, Goodea, Xenotaenia and Ilyodon, which, taken with evidence of positive selection, may indicate adaptive introgression of genes involved in MHC II pathway. Recurrent positive selection on immune-related genes, particularly genes involved in MHC II pathway, have also been associated with the evolution of viviparity in pipefish and seahorses (Roth et al 2020), and broadly across Cyprinodontiformes (Yusuf et al 2023).…”

Section: Discussionmentioning

confidence: 99%

Evidence for gene flow and trait reversal during radiation of Mexican Goodeid fish

Yusuf,

Lemus,

Thorpe

et al. 2024

Heredity

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Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. The Goodeinae are a group of live-bearing fishes endemic to Mexico. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four Goodeinae species, including Ataeniobius toweri, the only matrotrophic live-bearing fish without a trophotaenia in the group. We estimated timings of species divergence and examined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We used branch-site models to detect genome-wide positive selection across Goodeinae, and we specifically asked whether this differs in A. toweri, where loss of placental viviparity has recently occurred. We found evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, and gene flow may explain previous uncertainties about Goodeid phylogeny. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism-driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae.

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Section: Discussionmentioning

confidence: 99%

Evidence for gene flow and trait reversal during radiation of Mexican Goodeid fish

Yusuf,

Lemus,

Thorpe

et al. 2024

Heredity

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“…Positive selection on immune response genes has been shown to be a relatively common feature of surveys of positive selection across mammals, birds, and invertebrates (Jiggins and Kim, 2007;Kosiol et al, 2008;Shultz and Sackton, 2019) We also find evidence of introgression of genes involved in adaptive immune response between A. toweri and an ancestral lineage leading to the divergence of Ameca, Xenoophorus, Goodea, Xenotaenia and Ilyodon, which, taken with evidence of positive selection, may indicate adaptive introgression of genes involved in MHC II pathway. Recurrent positive selection on immune-related genes, particularly genes involved in MHC II pathway, have also been associated with the evolution of viviparity in pipefish and seahorses (Roth et al, 2020), and broadly across Cyprinodontiformes (Yusuf et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

Speciation on a complex landscape; phylogeny and demography of Mexican Goodeid fish

Yusuf

Lemus

Thorpe

et al. 2022

Preprint

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Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. Vicariance has clearly played a major role in diversification across diverse groups of organisms, but how this interacts with intrinsic biological features such as changes in reproductive system or sexual selection is less well understood. The Goodeinae are a Mexican endemic group of live-bearing fish. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four new Goodeinae genomes, including A. toweri, the only matrotrophic live-bearing fish without a trophotaenia in the group. We produced a phylogeny of the Goodeinae and estimate timings of species divergence. We determined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We also analyse patterns in the changes of effective population size for the species and examine the time course of expansion and decline. We used branch-site models to detect genome-wide positive selection across Goodeinae, and we specifically ask if this differs in A. toweri, where reversal of placental viviparity has recently occurred. We find that Goodeinae diverged rapidly, with reductions in effective population size after each split. Contrary to expectations, we find evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, potentially as a result of river piracy. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae.

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“…There are a variety of methods applied to detect convergent evolution at the same individual nucleotides (Hasselmann et al 2008), individual amino acids (Rey et al 2018;Thomas and Hahn 2015;Fukushima and Pollock 2023), regulatory elements (Partha et al 2017;Kowalczyk, Chikina, and Clark 2022;Kaplow et al 2023;Yan et al 2023), and genes (Kosakovsky Pond et al 2020;Kowalczyk et al 2019). These methods have been applied to identify convergent molecular evolution associated with a wide variety of traits in a wide number of clades (Yusuf et al 2023;Jin et al 2023).…”

Section: Introductionmentioning

confidence: 99%

RERconverge Expansion: Using Relative Evolutionary Rates to Study Complex Categorical Trait Evolution

Redlich,

Kowalczyk,

Tene

et al. 2023

Preprint

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Comparative genomics approaches seek to associate evolutionary genetic changes with the evolution of phenotypes across a phylogeny. Many of these methods, including our evolutionary rates based method, RERconverge, lack the capability of analyzing non-ordinal, multicategorical traits. To address this limitation, we introduce an expansion to RERconverge that associates shifts in evolutionary rates with the convergent evolution of multi-categorical traits. The categorical RERconverge expansion includes methods for performing categorical ancestral state reconstruction, statistical tests for associating relative evolutionary rates with categorical variables, and a new method for performing phylogenetic permulations on multi-categorical traits. In addition to demonstrating our new method on a three-category diet phenotype, we compare its performance to naive pairwise binary RERconverge analyses and two existing methods for comparative genomic analyses of categorical traits: phylogenetic simulations and a phylogenetic signal based method. We also present a diagnostic analysis of the new permulations approach demonstrating how the method scales with the number of species and the number of categories included in the analysis. Our results show that our new categorical method outperforms phylogenetic simulations at identifying genes and enriched pathways significantly associated with the diet phenotype and that the new ancestral reconstruction drives an improvement in our ability to capture diet-related enriched pathways. Our categorical permulations were able to account for non-uniform null distributions and correct for non-independence in gene rank during pathway enrichment analysis. The categorical expansion to RERconverge will provide a strong foundation for applying the comparative method to categorical traits on larger data sets with more species and more complex trait evolution.

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Genomic signatures associated with transitions to viviparity in Cyprinodontiformes

Cited by 3 publications

References 128 publications

Evidence for gene flow and trait reversal during radiation of Mexican Goodeid fish

Evidence for gene flow and trait reversal during radiation of Mexican Goodeid fish

Speciation on a complex landscape; phylogeny and demography of Mexican Goodeid fish

RERconverge Expansion: Using Relative Evolutionary Rates to Study Complex Categorical Trait Evolution

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