Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes

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.

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

International Journal of Ecology ◽

10.1155/2011/435357 ◽

2011 ◽

Vol 2011 ◽

pp. 1-15 ◽

Cited By ~ 24

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.

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

10.1101/698225 ◽

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.

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

10.1101/545103 ◽

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.

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

Molecular Biology and Evolution ◽

10.1093/molbev/msz259 ◽

2019 ◽

Vol 37 (3) ◽

pp. 695-710 ◽

Cited By ~ 2

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

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Long distance pollen-mediated gene flow at a landscape level: the weed beet as a case study

Molecular Ecology ◽

10.1111/j.1365-294x.2007.03448.x ◽

2007 ◽

Vol 16 (18) ◽

pp. 3801-3813 ◽

Cited By ~ 51

Author(s):

STÉPHANE FÉNART ◽

FRÉDÉRIC AUSTERLITZ ◽

JOËL CUGUEN ◽

JEAN-FRANÇOIS ARNAUD

Keyword(s):

Gene Flow ◽

Long Distance ◽

Landscape Level

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The effects of inbreeding, outbreeding and long-distance gene flow on survivorship in North American populations of Silene vulgaris

Journal of Ecology ◽

10.1111/j.1365-2745.2005.01090.x ◽

2006 ◽

Vol 94 (1) ◽

pp. 98-109 ◽

Cited By ~ 28

Author(s):

MAIA F. BAILEY ◽

DAVID E. McCAULEY

Keyword(s):

Gene Flow ◽

North American ◽

Silene Vulgaris ◽

Long Distance

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Camelina (Camelina sativa L. Crantz) Crop Performance, Insect Pollinators, and Pollen Dispersal in the Northeastern US

10.1101/756619 ◽

2019 ◽

Author(s):

Richard Rizzitello ◽

Chuan-Jie Zhang ◽

Carol Auer

Keyword(s):

Gene Flow ◽

Honey Bees ◽

Pollen Dispersal ◽

Camelina Sativa ◽

Genetically Engineered ◽

Oilseed Crop ◽

Crop Failure ◽

Long Distance ◽

Insect Visitation ◽

Pollinating Insects

AbstractCamelina sativa (camelina) is an oilseed crop in the Brassicaceae that has been genetically engineered for the production of biofuels, dietary supplements, and other industrial compounds. Cultivation in North America is both recent and limited, so there are gaps in knowledge regarding yield, weed competition, and pollen-mediated gene flow. For these experiments, camelina ‘SO-40’ was grown for three years without weed control. Spring-sown camelina was harvested at 80-88 days with ∼1200 growing degree days (GDD) with yields of 425-508 kg/hectare. Camelina yields were the same with or without weeds, showing competitive ability in low-management conditions. Crop failure in 2015 was associated with delayed rainfall and above-average temperatures after seeding. Camelina flowers attracted pollinating insects from the Hymenoptera, Diptera, Lepidoptera, and Coleoptera. Hymenoptera included honey bees (Apis melifera), mining bees (Andrenidae), sweat bees (Halictidae), bumble bees (Bombus spp.) and leaf cutter bees (Megachilidae). Insect visitation on camelina flowers was associated with modest increases in seed yield. Honey bees comprised 28-33% of all pollinators and were shown to carry camelina pollen on their legs. Air sampling showed that wind-blown pollen was present at low concentrations at 9 m beyond the edges of the field. These experiments demonstrated for the first time that camelina pollen dispersal could occur through honey bees or wind, although bee activity would likely be more significant for long-distance gene flow.

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Spatial population genomics of a recent mosquito invasion

10.1101/2020.11.30.405191 ◽

2020 ◽

Author(s):

Thomas L Schmidt ◽

T. Swan ◽

Jessica Chung ◽

Stephan Karl ◽

Samuel Demok ◽

...

Keyword(s):

Gene Flow ◽

Population Genomics ◽

Isolation By Distance ◽

Spatial Genetic Structure ◽

Nucleotide Polymorphisms ◽

Discrete Events ◽

Long Distance ◽

Population Genomic ◽

Asian Tiger ◽

Study Designs

AbstractPopulation genomic approaches can characterise dispersal across a single generation through to many generations in the past, bridging the gap between individual movement and intergenerational gene flow. These approaches are particularly useful when investigating dispersal in recently altered systems, where they provide a way of inferring long-distance dispersal between newly established populations and their interactions with existing populations. Human-mediated biological invasions represent such altered systems which can be investigated with appropriate study designs and analyses. Here we apply temporally-restricted sampling and a range of population genomic approaches to investigate dispersal in a 2004 invasion of Aedes albopictus (the Asian tiger mosquito) in the Torres Strait Islands (TSI) of Australia. We sampled mosquitoes from 13 TSI villages simultaneously and genotyped 373 mosquitoes at genome-wide single nucleotide polymorphisms (SNPs): 331 from the TSI, 36 from Papua New Guinea (PNG), and 4 incursive mosquitoes detected in uninvaded regions. Within villages, spatial genetic structure varied substantially but overall displayed isolation by distance and a neighbourhood size of 232–577. Close kin dyads revealed recent movement between islands 31–203 km apart, and deep learning inferences showed incursive Ae. albopictus had travelled to uninvaded regions from both adjacent and non-adjacent islands. Private alleles and a coancestry matrix indicated direct gene flow from PNG into nearby islands. Outlier analyses also detected four linked alleles introgressed from PNG, with the alleles surrounding 12 resistance-associated cytochrome P450 genes. By treating dispersal as both an intergenerational process and a set of discrete events, we describe a highly interconnected invasive system.

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The Genomic Architecture of a Rapid Island Radiation: Recombination Rate Variation, Chromosome Structure, and Genome Assembly of the Hawaiian Cricket Laupala

10.1101/160952 ◽

2017 ◽

Cited By ~ 1

Author(s):

Thomas Blankers ◽

Kevin P. Oh ◽

Aureliano Bombarely ◽

Kerry L. Shaw

Keyword(s):

Large Scale ◽

De Novo ◽

Chromosomal Rearrangements ◽

Evolutionary Genetics ◽

Rate Variation ◽

Linkage Maps ◽

Recombination Rates ◽

Behavioral Isolation ◽

Genomic Architecture ◽

Suppressed Recombination

ABSTRACTPhenotypic evolution and speciation depend on recombination in many ways. Within populations, recombination can promote adaptation by bringing together favorable mutations and decoupling beneficial and deleterious alleles. As populations diverge, cross-over can give rise to maladapted recombinants and impede or reverse diversification. Suppressed recombination due to genomic rearrangements, modifier alleles, and intrinsic chromosomal properties may offer a shield against maladaptive gene flow eroding co-adapted gene complexes. Both theoretical and empirical results support this relationship. However, little is known about this relationship in the context of behavioral isolation, where co-evolving signals and preferences are the major hybridization barrier. Here we examine the genomic architecture of recently diverged, sexually isolated Hawaiian swordtail crickets (Laupala). We assemble a de novo genome and generate three dense linkage maps from interspecies crosses. In line with expectations based on the species’ recent divergence and successful interbreeding in the lab, the linkage maps are highly collinear and show no evidence for large-scale chromosomal rearrangements. The maps were then used to anchor the assembly to pseudomolecules and estimate recombination rates across the genome. We tested the hypothesis that loci involved in behavioral isolation (song and preference divergence) are in regions of low interspecific recombination. Contrary to our expectations, a genomic region where a male song QTL co-localizes with a female preference QTL was not associated with particularly low recombination rates. This study provides important novel genomic resources for an emerging evolutionary genetics model system and suggests that trait-preference co-evolution is not necessarily facilitated by locally suppressed recombination.

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