Repeated genetic adaptation to high altitude in two tropical butterflies

Montejo‐Kovacevich, Gabriela; Meier, Joana I.; Bacquet, Caroline; Warren, Ian A.; Chan, Yingguang Frank; Kucka, Mareck; Salazar, Camilo; Rueda-M, Nicol; Montgomery, Stephen H.; McMillan, W. Owen; Kozak, Krzysztof M.; Nadeau, Nicola J.; Martin, Simon H.; Jiggins, Chris D.

doi:10.1101/2021.11.30.470630

Cited by 5 publications

(6 citation statements)

References 123 publications

(126 reference statements)

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“…For numerous traits, including plumage coloration, sexual dimorphism, and migration behavior, not related species display more similar phenotypes than sister species (Fig. 1 Furthermore, our results suggest (directly for introgression and ILS, indirectly for novel mutations) that convergent evolution in open-habitat chats is unlikely explained by a single process but may need to invoke all three processes (Hedrick 2013;Konečná et al 2021;Montejo-Kovacevich et al 2021;Natarajan et al 2015;Pease et al 2016), with the most likely processes depending on both demography and the phylogenetic scale.…”

Section: Diverse Routes To Convergent Evolution In Open-habitat Chatsmentioning

confidence: 63%

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

Kakhki

Schweizer

Lutgen

et al. 2022

Molecular Biology and Evolution

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Insights into the processes underpinning convergent evolution advance our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin convergent evolution. Here, we were interested in understanding the processes involved in convergent evolution in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the pattern of abundant convergent evolution, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for a role of novel mutations in the evolution of these phenotypes. Together, our results suggest that convergent evolution in open-habitat chats involved diverse processes and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.

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Section: Diverse Routes To Convergent Evolution In Open-habitat Chatsmentioning

confidence: 63%

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

Kakhki

Schweizer

Lutgen

et al. 2022

Molecular Biology and Evolution

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show abstract

“…Furthermore, our results suggest (directly for introgression and ILS, indirectly for novel mutations) that convergent evolution in open-habitat chats is unlikely explained by a single process but may need to invoke all three processes (Hedrick 2013; Konečná et al 2021; Montejo-Kovacevich et al 2021; Natarajan et al 2015; Pease et al 2016), with the most likely processes depending on both demography and the phylogenetic scale.…”

Section: Discussionmentioning

confidence: 81%

“…). Almost entirely black plumages, for instance, evolved in five clades (O. picata opistholeuca, O. warriae, O. leucura, female M. monticola, and juvenile O. leucopyga), and sexually monomorphic female-type plumage is found in another five clades (O. chrysopygia, O. fusca, the O. melanura clade, the O. isabellina clade, and in the sub-Saharan clade), to name just two out of many examples.Furthermore, our results suggest (directly for introgression and ILS, indirectly for novel mutations) that convergent evolution in open-habitat chats is unlikely explained by a single process but may need to invoke all three processes(Hedrick 2013;Konečná et al 2021;Montejo- Kovacevich et al 2021;Natarajan et al 2015;Pease et al 2016), with the most likely processes depending on both demography and the phylogenetic scale.…”

mentioning

confidence: 80%

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

Kakhki

Schweizer

Lutgen

et al. 2022

Preprint

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Insights into the processes underpinning the evolution of phenotypic parallelism contribute to our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin phenotypic parallelism. Here, we were interested in understanding the trajectories along which phenotypic parallelism may have evolved in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the evidence for abundant phenotypic parallelism, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for a role of novel mutations in the evolution of these phenotypes. Together, our results suggest that phenotypic parallelism in open-habitat chats evolved along diverse trajectories and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.

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“…It would also be worthwhile exploring the effect of standing genetic variation or migration in future studies. Standing genetic variation enables the parental populations to incorporate the same alleles when the environment changes, increasing parallelism (Montejo-Kovacevich et al 2021; Thompson et al 2019). Similarly, migration between parental populations allows the spread and fixation of the same favorable alleles.…”

Section: Discussionmentioning

confidence: 99%

The phoenix hypothesis of speciation

Yamaguchi

Wiley

Otto

2022

Preprint

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Genetic divergence among allopatric populations builds reproductive isolation over time and is thought to be the major mechanism underlying the formation of new species. This process is accelerated when populations face a changing environment, but abrupt change also places populations at risk of extinction. Here we use simulations of Fisher's geometric model with explicit population dynamics to explore the genetic changes that occur in the face of extreme environmental changes to which populations must adapt or go extinct. We show that evolutionary rescue leads to the fixation of mutations whose effects are larger on average and that these mutations are more likely to lead to reproductive isolation, compared with populations not at risk of extinction. We refer to the formation of new species from the ashes of populations in decline as the phoenix hypothesis of speciation. The phoenix hypothesis predicts more substantial hybrid fitness breakdown among populations surviving a higher extinction risk. The hypothesis was supported when many loci underlie adaptation. When, however, there was only a small number of potential rescue mutations, we found that mutations fixed in different populations were more likely to be identical, with parallel changes reducing isolation. With a limited genomic potential for adaptation, we find support for a modified version of the phoenix hypothesis where reproductive isolation builds fastest in populations subject to an intermediate extinction risk. While processes driving extinction lead to the loss of lineages with deep evolutionary histories, they may also generate new taxa, albeit taxa with minimal genetic differences.

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Repeated genetic adaptation to high altitude in two tropical butterflies

Cited by 5 publications

References 123 publications

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

The phoenix hypothesis of speciation

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