scholarly journals Divergent selection and primary gene flow shape incipient speciation of a riparian tree on Hawaii Island

2019 ◽  
Author(s):  
Jae Young Choi ◽  
Michael Purugganan ◽  
Elizabeth A. Stacy
Keyword(s):  
Gene Flow ◽  
Divergent Selection ◽  
Genomic Islands ◽  
Disruptive Selection ◽  
Metrosideros Polymorpha ◽  
Incipient Speciation ◽  
Island Endemic ◽  
Hawaii Island ◽  
Riparian Tree ◽  
Primary Gene

AbstractA long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within HawaiianMetrosideros, a hyper-variable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin ofMetrosideros polymorphavar.newellii(newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wideM. polymorphavar.glaberrima(glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii’s origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3-1.2 million years. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e.secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e.primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.Author summaryA long-standing question in evolution is whether or not new species can arise in the presence of gene flow, which is expected to inhibit the formation of reproductive isolating barriers. We investigated the genomics underlying the origin of a Hawaii Island-endemic riparian tree and purported case of incipient sympatric speciation due to disruptive selection across a sharp forest-riparian ecotone. We find extensive evidence of ongoing gene flow between the riparian tree and its closest relative along with local genomic regions resistant to admixture that likely formed through selection on genes for ecological adaptation and/or reproductive isolation. These results strongly suggest that where disruptive selection is strong, incipient speciation with gene flow is possible even in long-lived, highly dispersible trees.

scholarly journals Divergent Selection and Primary Gene Flow Shape Incipient Speciation of a Riparian Tree on Hawaii Island

2019 ◽  
Vol 37 (3) ◽  
pp. 695-710 ◽  
Author(s):  
Jae Young Choi ◽  
Michael Purugganan ◽  
Elizabeth A Stacy
Keyword(s):  
Gene Flow ◽  
Evolutionary Biology ◽  
Woody Species ◽  
Divergent Selection ◽  
Genomic Islands ◽  
Disruptive Selection ◽  
Metrosideros Polymorpha ◽  
Hawaii Island ◽  
Riparian Tree ◽  
Primary Gene

Abstract A long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within Hawaiian Metrosideros, a hypervariable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin of Metrosideros polymorpha var. newellii (newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wide M. polymorpha var. glaberrima (glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii’s origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3–1.2 My. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e., secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e., primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.

scholarly journals Theoretical Expression for the Evolution of Genomic Island of Speciation: From Its Birth to Preservation

2019 ◽  
Author(s):  
T. Sakamoto ◽  
H. Innan
Keyword(s):  
Genetic Variation ◽  
Gene Flow ◽  
Genetic Divergence ◽  
Genomic Island ◽  
Evolutionary Process ◽  
Ecological Speciation ◽  
Divergent Selection ◽  
Genomic Islands ◽  
Theoretical Expression ◽  
Locally Adaptive

AbstractEcological speciation could be driven by divergent selection that works to maintain phenotypes that are adaptive to each niche. In its early stages, genetic divergence (or FST) can be maintained around the target sites of divergent selection, while in other regions, genetic variation can be mixed by gene flow or migration. Such regions of elevated genetic divergence are called genomic islands of speciation. In this work, we theoretically consider the evolutionary process of a genomic island of speciation, from its birth to stable preservation. Under a simple two-population model, we use a diffusion approach to obtain analytical expressions for the probability of initial establishment of a locally adaptive allele, the reduction of genetic variation due to the spread of the adaptive allele, and the process to the development of a sharp peak of divergence. Our result would be useful to understand how genomes evolve through ecological speciation with gene flow.

scholarly journals Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes

2012 ◽  
Vol 367 (1587) ◽  
pp. 395-408 ◽  
Author(s):  
Paul A. Hohenlohe ◽  
Susan Bassham ◽  
Mark Currey ◽  
William A. Cresko
Keyword(s):  
Linkage Disequilibrium ◽  
Gene Flow ◽  
Fresh Water ◽  
Threespine Stickleback ◽  
Divergent Selection ◽  
Genomic Islands ◽  
Next Generation Sequencing Data ◽  
Rate Variation ◽  
Long Distance ◽  
Genomic Architecture

Population genomic studies are beginning to provide a more comprehensive view of dynamic genome-scale processes in evolution. Patterns of genomic architecture, such as genomic islands of increased divergence, may be important for adaptive population differentiation and speciation. We used next-generation sequencing data to examine the patterns of local and long-distance linkage disequilibrium (LD) across oceanic and freshwater populations of threespine stickleback, a useful model for studies of evolution and speciation. We looked for associations between LD and signatures of divergent selection, and assessed the role of recombination rate variation in generating LD patterns. As predicted under the traditional biogeographic model of unidirectional gene flow from ancestral oceanic to derived freshwater stickleback populations, we found extensive local and long-distance LD in fresh water. Surprisingly, oceanic populations showed similar patterns of elevated LD, notably between large genomic regions previously implicated in adaptation to fresh water. These results support an alternative biogeographic model for the stickleback radiation, one of a metapopulation with appreciable bi-directional gene flow combined with strong divergent selection between oceanic and freshwater populations. As predicted by theory, these processes can maintain LD within and among genomic islands of divergence. These findings suggest that the genomic architecture in oceanic stickleback populations may provide a mechanism for the rapid re-assembly and evolution of multi-locus genotypes in newly colonized freshwater habitats, and may help explain genetic mapping of parallel phenotypic variation to similar loci across independent freshwater populations.

scholarly journals Ecological Divergence and the Origins of Intrinsic Postmating Isolation with Gene Flow

2011 ◽  
Vol 2011 ◽  
pp. 1-15 ◽  
Author(s):  
Aneil F. Agrawal ◽  
Jeffrey L. Feder ◽  
Patrik Nosil
Keyword(s):  
Linkage Disequilibrium ◽  
Gene Flow ◽  
Natural Selection ◽  
Theoretical Models ◽  
Ecological Speciation ◽  
Divergent Selection ◽  
Postmating Isolation ◽  
Divergent Natural Selection ◽  
Mathematical Exploration ◽  
Neutral Gene

The evolution of intrinsic postmating isolation has received much attention, both historically and in recent studies of speciation genes. Intrinsic isolation often stems from between-locus genetic incompatibilities, where alleles that function well within species are incompatible with one another when brought together in the genome of a hybrid. It can be difficult for such incompatibilities to originate when populations diverge with gene flow, because deleterious genotypic combinations will be created and then purged by selection. However, it has been argued that if genes underlying incompatibilities are themselves subject to divergent selection, then they might overcome gene flow to diverge between populations, resulting in the origin of incompatibilities. Nonetheless, there has been little explicit mathematical exploration of such scenarios for the origin of intrinsic incompatibilities during ecological speciation with gene flow. Here we explore theoretical models for the origin of intrinsic isolation where genes subject to divergent natural selection also affect intrinsic isolation, either directly or via linkage disequilibrium with other loci. Such genes indeed overcome gene flow, diverge between populations, and thus result in the evolution of intrinsic isolation. We also examine barriers to neutral gene flow. Surprisingly, we find that intrinsic isolation sometimes weakens this barrier, by impeding differentiation via ecologically based divergent selection.

Review Lecture Disruptive selection

1972 ◽  
Vol 182 (1067) ◽  
pp. 109-143 ◽  
Keyword(s):  
Gene Flow ◽  
Genetic Variance ◽  
Natural Populations ◽  
Disruptive Selection ◽  
Ecological Niches ◽  
Gene Exchange ◽  
Bisexual Species ◽  
Frequency Dependent ◽  
Ecological Conditions ◽  
Intermediate Phenotypes

A population is exposed to disruptive selection if more than one phenotype has optimal fitness and intermediate phenotypes have lower fitnesses. Maintenance of the two or more optima may depend upon their relative fitnesses being frequency dependent. Such selection may be expected in two contrasting types of situation. First the two or more optimal phenotypes may depend on one another as do the two sexes in a bisexual species. Secondly the optima may be set by heterogeneity of the environment. Then we may think in terms of a mosaic of ecological niches or a clinal situation, and may expect that gene flow will tend to promote convergence of the sub-populations while disruptive selection tends to promote their divergence. Disruptive selection may therefore be relevant both to the evolution and maintenance of polymorphisms and to the divergence of parts of populations one from another, under the influence of variation of ecological conditions within the range of gametic and/or zygotic dispersal. Disruptive selection has been shown to be capable of increasing phenotypic and genetic variance, of producing and maintaining polymorphisms, of causing divergence of sub-populations between which substantial gene exchange occurs, and of splitting a population into two which are genetically isolated from one another. These results are reviewed and their relevance to natural populations discussed.

scholarly journals Speciation with gene flow in marine systems

2019 ◽  
pp. 1-40
Author(s):  
Gerrit Potkamp ◽  
Charles H.J.M. Fransen
Keyword(s):  
Gene Flow ◽  
Current Knowledge ◽  
Large Body ◽  
Theoretical Models ◽  
Tropical Fish ◽  
Colour Pattern ◽  
Disruptive Selection ◽  
Marine Systems ◽  
Wide Range ◽  
Marine Realm

Over the last century, a large body of literature emerged on mechanisms driving speciation. Most of the research into these questions focussed on terrestrial systems, while research in marine systems lagged behind. Here, we review the population genetic mechanisms and geographic context of 33 potential cases of speciation with gene flow in the marine realm, using six criteria inferred from theoretical models of speciation. Speciation with gene flow occurs in a wide range of marine taxa. Single traits, which induce assortative mating and are subjected to disruptive selection, such as differences in host-associations in invertebrates or colour pattern in tropical fish, are potentially responsible for a decrease in gene flow and may be driving divergence in the majority of cases. However, much remains unknown, and with the current knowledge, the frequency of ecological speciation with gene flow in marine systems remains difficult to estimate. Standardized, generally applicable statistical methods, explicitly testing different hypotheses of speciation, are, going forward, required to confidently infer speciation with gene flow.

scholarly journals Sharing of chloroplast haplotypes among red oak species suggests interspecific gene flow between neighboring populations

Botany ◽  
2015 ◽  
Vol 93 (10) ◽  
pp. 691-700 ◽  
Author(s):  
Ruhua Zhang ◽  
Andrew L. Hipp ◽  
Oliver Gailing
Keyword(s):  
Gene Flow ◽  
Chloroplast Dna ◽  
Genetic Markers ◽  
Dna Markers ◽  
Divergent Selection ◽  
Red Oak ◽  
Interspecific Gene Flow ◽  
Red Oaks ◽  
Chloroplast Dna Markers ◽  
Chloroplast Haplotypes

The North American red oak species Quercus rubra L., Quercus ellipsoidalis E. J. Hill, Quercus velutina Lam., and Quercus coccinea Münchh. are morphologically similar and showed very low interspecific differentiation at most nuclear genetic markers in our earlier analyses (<10%). However, a few genetic markers showed interspecific differentiation values (up to 84%) above neutral expectations, a pattern of genomic divergence consistent with models of ecological speciation in the face of gene flow and strong divergent selection. Accordingly, these interfertile species are predicted to maintain differential adaptations to drought, while neutral regions of the genome appear to be homogenized by interspecific gene flow. According to this model of maintenance of species integrity by divergent selection with gene flow, we expect a sharing of chloroplast haplotypes between interspecific population pairs. We analyzed maternally inherited chloroplast DNA markers for the first time in interspecific populations of the red oaks (section Lobatae) to provide additional evidence for contemporary gene flow between Q. rubra and Q. ellipsoidalis and between Q. velutina and Q. ellipsoidalis. Very low interspecific differentiation (GST = 0.023), but pronounced genetic differentiation among populations from different regions (GST = 0.277) across species, and sharing of regional chloroplast haplotypes between species in sympatric and neighboring populations provided strong evidence for contemporary interspecific gene flow. The pattern of divergence at chloroplast DNA markers in red oaks suggests interspecific gene flow that resulted in a sharing of chloroplast types while the ecological and morphological distinctness of species was maintained.

scholarly journals What role does natural selection play in speciation?

2010 ◽  
Vol 365 (1547) ◽  
pp. 1825-1840 ◽  
Author(s):  
N. H. Barton
Keyword(s):  
Gene Flow ◽  
Habitat Preference ◽  
Genetic Variance ◽  
Bimodal Distribution ◽  
Biological Species ◽  
Disruptive Selection ◽  
Linkage Equilibrium ◽  
Sexual Population ◽  
Trade Off ◽  
High Gene

If distinct biological species are to coexist in sympatry, they must be reproductively isolated and must exploit different limiting resources. A two-niche Levene model is analysed, in which habitat preference and survival depend on underlying additive traits. The population genetics of preference and viability are equivalent. However, there is a linear trade-off between the chances of settling in either niche, whereas viabilities may be constrained arbitrarily. With a convex trade-off, a sexual population evolves a single generalist genotype, whereas with a concave trade-off, disruptive selection favours maximal variance. A pure habitat preference evolves to global linkage equilibrium if mating occurs in a single pool, but remarkably, evolves to pairwise linkage equilibrium within niches if mating is within those niches—independent of the genetics. With a concave trade-off, the population shifts sharply between a unimodal distribution with high gene flow and a bimodal distribution with strong isolation, as the underlying genetic variance increases. However, these alternative states are only simultaneously stable for a narrow parameter range. A sharp threshold is only seen if survival in the ‘wrong’ niche is low; otherwise, strong isolation is impossible. Gene flow from divergent demes makes speciation much easier in parapatry than in sympatry.

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