PARALLEL EVOLUTION OF LOCAL ADAPTATION AND REPRODUCTIVE ISOLATION IN THE FACE OF GENE FLOW

Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky–Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that many incipient species may initially face. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

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The Evolutionary History of Nebraska Deer Mice: Local Adaptation in the Face of Strong Gene Flow

Molecular Biology and Evolution ◽

10.1093/molbev/msy004 ◽

2018 ◽

Vol 35 (4) ◽

pp. 792-806 ◽

Cited By ~ 33

Author(s):

Susanne P Pfeifer ◽

Stefan Laurent ◽

Vitor C Sousa ◽

Catherine R Linnen ◽

Matthieu Foll ◽

...

Keyword(s):

Gene Flow ◽

Local Adaptation ◽

Evolutionary History ◽

Deer Mice ◽

The Face ◽

History Of

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The limits to parapatric speciation 3: Evolution of strong reproductive isolation in presence of gene flow despite limited ecological differentiation

10.1101/2020.02.19.956292 ◽

2020 ◽

Cited By ~ 1

Author(s):

Alexandre Blanckaert ◽

Claudia Bank ◽

Joachim Hermisson

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Local Adaptation ◽

Maximum Amount ◽

Genetic Barrier ◽

Incipient Species ◽

Postzygotic Reproductive Isolation ◽

Minimal Configuration ◽

Parapatric Speciation ◽

Two Populations

AbstractGene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky-Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that may initially face many incipient species. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation.

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Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.1493 ◽

2010 ◽

Vol 278 (1705) ◽

pp. 511-518 ◽

Cited By ~ 79

Author(s):

Richard M. Merrill ◽

Bas Van Schooten ◽

Janet A. Scott ◽

Chris D. Jiggins

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Hybrid Sterility ◽

Mate Recognition ◽

Colour Pattern ◽

Genetic Associations ◽

Male Preference ◽

Heliconius Melpomene ◽

The Face ◽

Heliconius Cydno

Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene , also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which ‘speciation genes’ are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.

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The impact of global selection on local adaptation and reproductive isolation

10.1101/855320 ◽

2019 ◽

Cited By ~ 1

Author(s):

Gertjan Bisschop ◽

Derek Setter ◽

Marina Rafajlović ◽

Stuart J.E. Baird ◽

Konrad Lohse

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Local Adaptation ◽

Genetic Load ◽

Divergent Selection ◽

Mutation Process ◽

Genome Wide ◽

The Impact ◽

Two Populations ◽

Global Selection

AbstractDespite the homogenising effect of strong gene flow between two populations, adaptation under symmetric divergent selection pressures results in partial reproductive isolation: adaptive substitutions act as local barriers to gene flow, and if divergent selection continues unimpeded, this will result in complete reproductive isolation of the two populations, i.e. speciation. However, a key issue in framing the process of speciation as a tension between local adaptation and the homogenising force of gene flow is that the mutation process is blind to changes in the environment and therefore tends to limit adaptation. Here we investigate how globally beneficial mutations (GBMs) affect divergent local adaptation and reproductive isolation. When phenotypic divergence is finite, we show that the presence of GBMs limits local adaptation, generating a persistent genetic load at the loci which contribute to the trait under divergent selection and reducing genome-wide divergence. Furthermore, we show that while GBMs cannot prohibit the process of continuous differentiation, they induce a substantial delay in the genome-wide shutdown of gene flow.

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The impact of global selection on local adaptation and reproductive isolation

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0531 ◽

2020 ◽

Vol 375 (1806) ◽

pp. 20190531 ◽

Cited By ~ 2

Author(s):

Gertjan Bisschop ◽

Derek Setter ◽

Marina Rafajlović ◽

Stuart J. E. Baird ◽

Konrad Lohse

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Local Adaptation ◽

Genetic Load ◽

Divergent Selection ◽

Mutation Process ◽

Genome Wide ◽

The Impact ◽

Two Populations ◽

Global Selection

Despite the homogenizing effect of strong gene flow between two populations, adaptation under symmetric divergent selection pressures results in partial reproductive isolation: adaptive substitutions act as local barriers to gene flow, and if divergent selection continues unimpeded, this will result in complete reproductive isolation of the two populations, i.e. speciation. However, a key issue in framing the process of speciation as a tension between local adaptation and the homogenizing force of gene flow is that the mutation process is blind to changes in the environment and therefore tends to limit adaptation. Here we investigate how globally beneficial mutations (GBMs) affect divergent local adaptation and reproductive isolation. When phenotypic divergence is finite, we show that the presence of GBMs limits local adaptation, generating a persistent genetic load at the loci that contribute to the trait under divergent selection and reducing genome-wide divergence. Furthermore, we show that while GBMs cannot prohibit the process of continuous differentiation, they induce a substantial delay in the genome-wide shutdown of gene flow. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

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Clustering of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies

10.1101/2020.06.03.131557 ◽

2020 ◽

Author(s):

Kelsey J. R. P. Byers ◽

Kathy Darragh ◽

Sylvia Fernanda Garza ◽

Diana Abondano Almeida ◽

Ian A. Warren ◽

...

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Genetic Architecture ◽

Color Pattern ◽

Chromosome 8 ◽

Pheromone Biosynthesis ◽

Chromosome 20 ◽

Backcross Hybrids ◽

The Face ◽

Pheromone Compound

AbstractThe degree to which loci promoting reproductive isolation cluster in the genome – i.e. the genetic architecture of reproductive isolation - can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously-produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male-transferred anti-aphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.

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Use of Genomic Resources to Assess Adaptive Divergence and Introgression in Oaks

Forests ◽

10.3390/f12060690 ◽

2021 ◽

Vol 12 (6) ◽

pp. 690

Author(s):

Desanka Lazic ◽

Andrew L. Hipp ◽

John E. Carlson ◽

Oliver Gailing

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Model Organisms ◽

Future Research ◽

Adaptive Divergence ◽

Natural Habitats ◽

Adaptive Introgression ◽

The Face ◽

Species Integrity

Adaptive divergence is widely accepted as a contributor to speciation and the maintenance of species integrity. However, the mechanisms leading to reproductive isolation, the genes involved in adaptive divergence, and the traits that shape the adaptation of wild species to changes in climate are still largely unknown. In studying the role of ecological interactions and environment-driven selection, trees have emerged as potential model organisms because of their longevity and large genetic diversity, especially in natural habitats. Due to recurrent gene flow among species with different ecological preferences, oaks arose as early as the 1970s as a model for understanding how speciation can occur in the face of interspecific gene flow, and what we mean by “species” when geographically and genomically heterogeneous introgression seems to undermine species’ genetic coherence. In this review, we provide an overview of recent research into the genomic underpinnings of adaptive divergence and maintenance of species integrity in oaks in the face of gene flow. We review genomic and analytical tools instrumental to better understanding mechanisms leading to reproductive isolation and environment-driven adaptive introgression in oaks. We review evidence that oak species are genomically coherent entities, focusing on sympatric populations with ongoing gene flow, and discuss evidence for and hypotheses regarding genetic mechanisms linking adaptive divergence and reproductive isolation. As the evolution of drought- and freezing-tolerance have been key to the parallel diversification of oaks, we investigate the question of whether the same or a similar set of genes are involved in adaptive divergence for drought and stress tolerance across different taxa and sections. Finally, we propose potential future research directions on the role of hybridization and adaptive introgression in adaptation to climate change.

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