Convergent evolution in the genomics era: new insights and directions

Sackton, Timothy B.; Clark, Nathan L.

doi:10.1098/rstb.2019.0102

Cited by 99 publications

(65 citation statements)

References 38 publications

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“…Emergence of non-parallel traits in response to local adaptation is less likely due to overall lower phenotypic variation among the alpine populations and very similar environmental conditions across alpine sites, speaking against strong selection triggered by locally-specific conditions. As parallelism informs about the role of selection, its detection is usually the prime aim of most studies (56), although the regionally-specific deviations provide valuable information on additional evolutionary processes affecting the predictability of evolution (8). Such inquiry, however, requires the study of multiple population pairs that evolved in parallela case that has been so far documented in only a handful of plant species (14,19).…”

Section: The Degree and Sources Of Non-parallelismmentioning

confidence: 99%

Parallel alpine differentiation inArabidopsis arenosa

Knotek

Konečná

Wos

et al. 2020

Preprint

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Parallel evolution provides powerful natural experiments for studying repeatability of evolution. Well-documented examples from plants are, however, still rare, as are inquiries of mechanisms driving convergence in some traits while divergence in others. Arabidopsis arenosa, a predominantly foothill species with scattered morphologically distinct alpine occurrences is a promising candidate. Yet, the hypothesis of parallelism remained untested. We sampled foothill and alpine populations in all regions known to harbour the alpine ecotype and used SNP genotyping to test for repeated alpine colonisation. Then, we combined field surveys and a common garden experiment to quantify phenotypic parallelism. Genetic clustering by region but not elevation and coalescent simulations demonstrated parallel origin of alpine ecotype in four mountain regions. Alpine populations exhibited parallelism in height and floral traits which persisted after two generations in cultivation. In contrast, leaf traits were distinctive only in certain region(s), reflecting a mixture of plasticity and genetically determined non-parallelism. We demonstrate varying degrees and causes of parallelism and nonparallelism across populations and traits within a plant species. Parallel divergence along a sharp elevation gradient makes A. arenosa a promising candidate for studying genomic basis of adaptation.

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Section: The Degree and Sources Of Non-parallelismmentioning

confidence: 99%

Parallel alpine differentiation inArabidopsis arenosa

Knotek

Konečná

Wos

et al. 2020

Preprint

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“…Convergent phenotypic evolution is a striking and often-observed phenomenon. The extent to which phenotypic convergence is driven by molecular convergence is a fascinating question with implications on our understanding of the constraints and predictability of species evolution (13). This question is complicated by the fact that convergent lineages do not necessarily show an overall excess of convergent genomic events (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Our recent ability to apply whole-genome sequencing to explore the genetic basis of natural complex adaptations (e.g., Fig. 1A) calls for the development of more systematic approaches for identifying adaptive molecular convergence patterns across genomes (11)(12)(13)(14). Recent genome-wide screens illuminated sensory genes with sequence changes that segregate with echolocating mammals (11).…”

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confidence: 99%

A functional enrichment test for molecular convergent evolution finds a clear protein-coding signal in echolocating bats and whales

Marcovitz

Turakhia

Chen

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Distantly related species entering similar biological niches often adapt by evolving similar morphological and physiological characters. How much genomic molecular convergence (particularly of highly constrained coding sequence) contributes to convergent phenotypic evolution, such as echolocation in bats and whales, is a long-standing fundamental question. Like others, we find that convergent amino acid substitutions are not more abundant in echolocating mammals compared to their outgroups. However, we also ask a more informative question about the genomic distribution of convergent substitutions by devising a test to determine which, if any, of more than 4,000 tissue-affecting gene sets is most statistically enriched with convergent substitutions. We find that the gene set most overrepresented (q-value = 2.2e-3) with convergent substitutions in echolocators, affecting 18 genes, regulates development of the cochlear ganglion, a structure with empirically supported relevance to echolocation. Conversely, when comparing to nonecholocating outgroups, no significant gene set enrichment exists. For aquatic and high-altitude mammals, our analysis highlights 15 and 16 genes from the gene sets most affected by molecular convergence which regulate skin and lung physiology, respectively. Importantly, our test requires that the most convergence-enriched set cannot also be enriched for divergent substitutions, such as in the pattern produced by inactivated vision genes in subterranean mammals. Showing a clear role for adaptive protein-coding molecular convergence, we discover nearly 2,600 convergent positions, highlight 77 of them in 3 organs, and provide code to investigate other clades across the tree of life.

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“…Biologists have long been fascinated by the convergent evolution of similar traits in distant lineages 1 . Given the tractability of population-based resequencing studies to detect candidate mechanisms underlying adaptations, the genomic underpinnings of convergence are increasingly coming to light 2 . Diverse examples can be found in all kingdoms, from the convergent basis for the loss in flight in birds 3 , to the evolution of toxin-resistant herbivory in insects 4 , to drug resistance in pathogens 5 .…”

Section: Introductionmentioning

confidence: 99%

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Bray

Wolf

Zhou

et al. 2020

Preprint

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Convergent evolution is observed broadly across the web of life, but the degree of evolutionary constraint during adaptation of core intracellular processes is not known. High constraint has been assumed for conserved processes, such as cell division and DNA repair, but reports of nimble evolutionary shifts in these processes have confounded this expectation. Whole genome duplication (WGD) necessitates the concerted adjustment of a wide range of fundamental intracellular functions but nevertheless has been repeatedly survived in all kingdoms. Given this repeated adaptation to WGD despite obvious intracellular challenges to core processes such as meiosis, we asked: how do lineages not only survive WGD, but sometimes ultimately thrive? Are the solutions employed constrained or diverse? Here we detect genes and processes under selection following WGD in the Cochlearia species complex by performing a scan for selective sweeps following WGD in a large-scale survey of 73 resequenced individuals from 23 populations across Europe. We then contrast our results from two independent WGDs in Arabidopsis arenosa and Cardamine amara. We find that while WGD does require the adaptation of particular functional processes in all three cases, the specific genes recruited to respond are highly flexible. We also observe evidence of varying degrees of convergence between different cases. Our results point to a polygenic basis for the distributed adaptive systems that control meiotic crossover number, ionomic rewiring, cell cycle control, and nuclear regulation. Given the sheer number of loci under selection post-WGD, we surmise that this polygenicity may explain the general lack of convergence between these species that are ~30 million years diverged. Based on our results, we speculate that adaptive processes themselves – such as the rate of generation of structural genomic variants—may be altered by WGD in nascent autopolyploids, contributing to the occasionally spectacular adaptability of autopolyploids observed across kingdoms.

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Convergent evolution in the genomics era: new insights and directions

Abstract: One contribution of 16 to a theme issue 'Convergent evolution in the genomics era: new insights and directions'.

Cited by 99 publications

References 38 publications

Parallel alpine differentiation inArabidopsis arenosa

Parallel alpine differentiation inArabidopsis arenosa

A functional enrichment test for molecular convergent evolution finds a clear protein-coding signal in echolocating bats and whales

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

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