Inter-chromosomal coupling between vision and pigmentation genes during genomic divergence

Hench, Kosmas; Vargas, Marta; Höppner, Marc P.; McMillan, W. Owen; Puebla, Oscar

doi:10.1038/s41559-019-0814-5

Cited by 55 publications

(86 citation statements)

References 107 publications

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“…Importantly, the genomic regions inferred to be under divergent selection were not shared across species. These results contrast with reported evidence of genomic convergence observed in parallel evolution (Jones et al, 2012;Ravinet et al, 2016), and evolutionary radiations (Hench et al, 2019;Muschick et al, 2012;Stryjewski and Sorenson, 2017). Our results suggest that recent and independent replicates of ecological divergence resulted in limited convergence due to the absence of shared genetic variation, complex and species-specific genomic architecture of traits under selection, and the recent timing of divergence, which may have prevented background selection to lead to similar signatures of selection (Burri, 2017).…”

Section: Resultscontrasting

confidence: 99%

“…The second concerns ecological radiation following the colonization of underutilized niches by a single species (Seehausen, 2004). These frameworks have identified several cases of evolutionary convergence underlined by similar genetic pathways across a suite of organisms (Hench et al, 2019;Hohenlohe et al, 2010;Lamichhaney et al, 2015;Muschick et al, 2012;Ravinet et al, 2016). The inferences from genome-wide variation has recently highlighted the role of gene flow between recently diverged species as a fuel for evolutionary radiations (Malinsky et al, 2018;Meier et al, 2017), as well as selection on standing variation to promote the parallel evolution of ecotypes (Belleghem et al, 2018;Marques et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Beyond parallel evolution: when several species colonize the same environmental gradient

Moan

Gaggiotti

Henriques

et al. 2019

Preprint

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Genomic signatures associated with population divergence, speciation and the evolutionary mechanisms responsible for these are key research topics in evolutionary biology.Evolutionary radiations and parallel evolution have offered opportunities to study the role of the environment by providing replicates of ecologically driven speciation. Here, we apply an extension of the parallel evolution framework to study replicates of ecological speciation where multiple species went through a process of population divergence during the colonization of a common environmental gradient. We used the conditions offered by the North Sea -Baltic Sea environmental transition zone and found clear evidence of population structure linked to the Baltic Sea salinity gradient in four flatfish species. We found highly heterogeneous signatures of population divergence within and between species, and no evidence of parallel genomic architecture across species associated with the divergence.Analyses of demographic history suggest that Baltic Sea lineages are older than the age of the Baltic Sea itself. In most cases, divergence appears to involve reticulated demography through secondary contact, and our analyses revealed that genomic patterns of divergence were likely the result of a combination of effects from past isolation and subsequent adaptation to a new environment. In one case, we identified two large structural variants associated with the environmental gradient, where populations were inferred to have diverged in the presence of gene flow. Our results highlight the heterogeneous genomic effects associated with complex interplays of evolutionary forces, and stress the importance of genomic background for studies of parallel evolution. 2006), but so far the comparative framework has not been extended with the use of higher genome coverage.Here, we used a comparative population genomic approach to study the evolutionary processes involved during the colonization of the Baltic Sea. We studied population structure of four closely related (but genetically isolated) flatfish species: turbot (Scophthalmus maximus), common dab (Limanda limanda), European plaice (Pleuronectes platessa) andEuropean flounder (Platichthys flesus). These species were considered replicates of population divergence and were analysed independently. Our analyses showed heterogeneous genetic patterns of North Sea (NS) -Baltic Sea (BS) differentiation across species, both for magnitudes and genomic patterns of differentiation. Most of the genetic differences found were strongly associated with the environmental gradient of the NBTZ.However, the majority of the genomic regions underlying the NS-BS divergence were not shared between species. The timing of divergence between NS-BS populations was inferred to be five to ten times older than the age of the Baltic Sea. In three species, population divergence was inferred to involve past isolation followed by a secondary contact phase, and our analyses revealed that highly diverged genomic regions were likely the result of ...

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Section: Resultscontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Beyond parallel evolution: when several species colonize the same environmental gradient

Moan

Gaggiotti

Henriques

et al. 2019

Preprint

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“…The restricted range of the Maya hamlet contrasts sharply with the pan‐Caribbean barred ( H. puella ), black ( H. nigricans ), and butter ( H. unicolor ) hamlets, which are also found in the coastal lagoon of the MBRS in Belize (Holt, Côté, & Emerson, ; Figure ). These species are sympatric throughout most of their range, with ongoing gene flow maintaining low levels of genetic differentiation despite strong assortative mating (Hench, Vargas, Höppner, McMillan, & Puebla, ; Puebla, Bermingham, Guichard, & Whiteman, ; Puebla, Bermingham, & McMillan, ). More broadly, the genus includes a total of 19 species that vary widely in range size and abundance (Holt et al, ).…”

Section: Introductionmentioning

confidence: 99%

The evolution of microendemism in a reef fish (Hypoplectrus maya)

et al. 2019

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Marine species tend to have extensive distributions, which are commonly attributed to the dispersal potential provided by planktonic larvae and the rarity of absolute barriers to dispersal in the ocean. Under this paradigm, the occurrence of marine microendemism without geographic isolation in species with planktonic larvae poses a dilemma. The recently described Maya hamlet (Hypoplectrus maya, Serranidae) is exactly such a case, being endemic to a 50‐km segment of the Mesoamerican Barrier Reef System (MBRS). We use whole‐genome analysis to infer the demographic history of the Maya hamlet and contrast it with the sympatric and pan‐Caribbean black (H. nigricans), barred (H. puella) and butter (H. unicolor) hamlets, as well as the allopatric but phenotypically similar blue hamlet (H. gemma). We show that H. maya is indeed a distinct evolutionary lineage, with genomic signatures of inbreeding and a unique demographic history of continuous decrease in effective population size since it diverged from congeners just ~3,000 generations ago. We suggest that this case of microendemism may be driven by the combination of a narrow ecological niche and restrictive oceanographic conditions in the southern MBRS, which is consistent with the occurrence of an unusually high number of marine microendemics in this region. The restricted distribution of the Maya hamlet, its decline in both census and effective population sizes, and the degradation of its habitat place it at risk of extinction. We conclude that the evolution of marine microendemism can be a fast and dynamic process, with extinction possibly occurring before speciation is complete.

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“…Teleost fish provide well-established model systems to reveal processes of diversification, including the impact of hybridization on speciation (e.g., Malinsky et al, 2018a; Hench et al 2019). A particularly promising system for hybridization research are catadromous freshwater eels of the genus Anguilla , one of the most species-rich genera of eels with high economic value (Nelson et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Stable Species Boundaries Despite Ten Million Years of Hybridization in Tropical Eels

Barth

Gubili²,

Matschiner

et al. 2019

Preprint

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1Genomic evidence is increasingly underpinning that hybridization between taxa is commonplace, 2 challenging our views on the mechanisms that maintain their boundaries. Here, we focus on seven 3 catadromous eel species (genus Anguilla), and use genome-wide sequence data from more than 450 4 individuals sampled across the tropical Indo-Pacific, morphological information, and three newly 5 assembled draft genomes to compare contemporary patterns of hybridization with signatures of 6 past gene flow across a time-calibrated phylogeny. We show that the seven species have remained 7 distinct entities for up to 10 million years, despite a dynamic scenario of incomplete isolation 8 whereby the current frequencies of hybridization across species pairs (over 5% of all individuals 9 were either F1 hybrids or backcrosses) contrast remarkably with patterns of past introgression. 10Based on near-complete asymmetry in the directionality of hybridization and decreasing frequencies 11 of later-generation hybrids, we identify cytonuclear incompatibilities and hybrid breakdown as two 12 powerful mechanisms that can support species cohesion even when hybridization has been pervasive 13 throughout the evolutionary history of entire clades. 14 Introduction 17The turn of the century has witnessed a paradigm shift in how we view the role of hybridization 18 for building up biological diversity. While hybridization was previously assumed to be spatially 19 restricted and confined to a small number of taxa, it became gradually recognized that incomplete 20 isolation of genomes is widespread across eukaryotes, with varied effects on adaptation and speci-21 ation (Mallet, 2005(Mallet, , 2007 Abbott et al., 2013; Taylor and Larson, 2019). More recently, this view 22 has been further fuelled by technical and analytical advances which enable the quantification of past 23 introgression, the genetic exchange through hybridization, across entire clades, revealing that it is 24 often the most rapidly radiating clades that experienced high frequencies of gene exchange (Meier 25 et al., 2017; Lamichhaney et al., 2018; Kozak et al., 2018; Edelman et al., 2018). This seemingly 26 paradoxical association between introgression and rapid species proliferation underlies a key ques-27 tion in evolutionary biology: How can species in diversifying clades be accessible for introgression 28 but nevertheless solidify their species boundaries? To answer this question, insights are required 29 into the mechanisms that gradually reduce the degree to which hybridization generates introgres-30 sion; however, these mechanisms are still poorly understood because contemporary hybridization 31 and past introgression have so far not been jointly studied and compared across multiple pairs of 32 animal species with different divergence times within a single clade.33 Teleost fish provide well-established model systems to reveal processes of diversification, includ-34 ing the impact of hybridization on speciation (e.g., Malinsky et al., 2018a; Hench et al. 2019).35 A partic...

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Inter-chromosomal coupling between vision and pigmentation genes during genomic divergence

Cited by 55 publications

References 107 publications

Beyond parallel evolution: when several species colonize the same environmental gradient

Beyond parallel evolution: when several species colonize the same environmental gradient

The evolution of microendemism in a reef fish (Hypoplectrus maya)

Stable Species Boundaries Despite Ten Million Years of Hybridization in Tropical Eels

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