The genomic landscape at a late stage of stickleback speciation: high genomic divergence interspersed by small localized regions of introgression

AbstractSpeciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Genomic studies on young species pairs have often revealed peaks of divergence and heterogeneous genomic differentiation. Yet it remains unclear how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation with gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little known of the genomic signatures of divergence and introgression in older systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to hybridise at a low rate throughout divergence. Population genomic data revealed that high levels of genomic differentiation are maintained across the majority of the genome when gene flow occurs. However despite this, we identified multiple, small regions of introgression, strongly correlated with recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.Author summaryWhen species evolve, reproductive isolation leads to a build-up of differentiation in the genome where genes involved in the process occur. Much of our understanding of this comes from early stage speciation, with relatively few examples from more divergent species pairs that still exchange genes. To address this, we focused on Pacific Ocean and Japan Sea sticklebacks, which co-occur in the Japanese islands. We established that they are the oldest and most divergent known stickleback species pair, that they evolved in the face of gene flow and that this gene flow is still on going. We found introgression is confined to small, localised genomic regions where recombination rate is high. Our results show high divergence can be maintained between species, despite extensive gene flow.

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High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species

eLife ◽

10.7554/elife.02535 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 62

Author(s):

Molly Schumer ◽

Rongfeng Cui ◽

Daniel L Powell ◽

Rebecca Dresner ◽

Gil G Rosenthal ◽

...

Keyword(s):

Gene Flow ◽

High Resolution ◽

Wide Distribution ◽

Epistatic Interactions ◽

High Resolution Mapping ◽

Swordtail Fish ◽

Genome Wide ◽

Genomic Divergence ◽

Resolution Mapping ◽

Genomic Regions

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species.

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Contrasting signatures of genomic divergence during sympatric speciation

Nature ◽

10.1038/s41586-020-2845-0 ◽

2020 ◽

Vol 588 (7836) ◽

pp. 106-111 ◽

Cited By ~ 1

Author(s):

Andreas F. Kautt ◽

Claudius F. Kratochwil ◽

Alexander Nater ◽

Gonzalo Machado-Schiaffino ◽

Melisa Olave ◽

...

Keyword(s):

Gene Flow ◽

Genetic Architecture ◽

Single Species ◽

Sympatric Speciation ◽

Ecological Performance ◽

Genome Wide ◽

Genomic Divergence ◽

Empirical Tests ◽

Selected Traits ◽

Stable Genome

AbstractThe transition from ‘well-marked varieties’ of a single species into ‘well-defined species’—especially in the absence of geographic barriers to gene flow (sympatric speciation)—has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.

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Population Genomic Evidence Reveals Subtle Patterns of Differentiation in the Trophically Polymorphic Cuatro Ciénegas Cichlid, Herichthys minckleyi

Journal of Heredity ◽

10.1093/jhered/esz004 ◽

2019 ◽

Vol 110 (3) ◽

pp. 361-369 ◽

Cited By ~ 1

Author(s):

Katherine L Bell ◽

Chris C Nice ◽

Darrin Hulsey

Keyword(s):

Gene Flow ◽

Biological Diversity ◽

Molecular Genetic ◽

Molecular Ecology ◽

Cichlid Fish ◽

Genome Wide ◽

A Genome ◽

The Face ◽

Or Gene ◽

Herichthys Minckleyi

Abstract In recent decades, an increased understanding of molecular ecology has led to a reinterpretation of the role of gene flow during the evolution of reproductive isolation and biological novelty. For example, even in the face of ongoing gene flow strong selection may maintain divergent polymorphisms, or gene flow may introduce novel biological diversity via hybridization and introgression from a divergent species. Herein, we elucidate the evolutionary history and genomic basis of a trophically polymorphic trait in a species of cichlid fish, Herichthys minckleyi. We explored genetic variation at 3 hierarchical levels; between H. minckleyi (n = 69) and a closely related species Herichthys cyanoguttatus (n = 10), between H. minckleyi individuals from 2 geographic locations, and finally between individuals with alternate morphotypes at both a genome-wide and locus-specific scale. We found limited support for the hypothesis that the H. minckleyi polymorphism is the result of ongoing hybridization between the 2 species. Within H. minckleyi we found evidence of geographic genetic structure, and using traditional population genetic analyses found that individuals of alternate morphotypes within a pool appear to be panmictic. However, when we used a locus-specific approach to examine the relationship between multi-locus genotype, tooth size, and geographic sampling, we found the first evidence for molecular genetic differences between the H. minckleyi morphotypes.

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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1713288114 ◽

2017 ◽

Vol 115 (2) ◽

pp. E236-E243 ◽

Cited By ~ 45

Author(s):

Tao Ma ◽

Kun Wang ◽

Quanjun Hu ◽

Zhenxiang Xi ◽

Dongshi Wan ◽

...

Keyword(s):

Gene Flow ◽

Species Complex ◽

Populus Euphratica ◽

Genomic Islands ◽

Ecological Selection ◽

Poplar Trees ◽

Genomic Divergence ◽

Genome Divergence ◽

Genomic Regions ◽

Time Of Divergence

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.

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Selection on a pleiotropic color gene block underpins early differentiation between two warbler species

10.1101/853390 ◽

2019 ◽

Cited By ~ 4

Author(s):

Silu Wang ◽

Sievert Rohwer ◽

Devin R. de Zwaan ◽

David P. L Toews ◽

Irby J. Lovette ◽

...

Keyword(s):

Gene Flow ◽

Genetic Basis ◽

Early Stage ◽

Population Substructure ◽

Carotenoid Pigment ◽

Single Nucleotide ◽

Gene Block ◽

Genome Wide ◽

Genomic Regions ◽

Divergence With Gene Flow

AbstractWhen one species gradually splits into two, divergent selection on specific traits can cause peaks of differentiation in the genomic regions encoding those traits. Whether speciation is initiated by strong selection on a few genomic regions with large effects or by more diffused selection on many regions with small effects remains controversial. Differentiated phenotypes between differentiating lineages are commonly involved in reproductive isolation, thus their genetic underpinnings are key to the genomics architecture of speciation. When two species hybridize, recombination over multiple generations can help reveal the genetic regions responsible for the differentiated phenotypes against a genomic background that has been homogenized via backcrossing and introgression. We used admixture mapping to investigate genomic differentiation and the genetic basis of differentiated plumage features (relative melanin and carotenoid pigment) between hybridizing sister species in the early stage of speciation: Townsend’s (Setophaga townsendi) and Hermit warblers (S. occidentalis). We found a few narrow and dispersed divergent regions between allopatric parental populations, consistent with the ‘divergence with gene flow’ model of speciation. One of the divergent peaks involves three genes known to affect pigmentation: ASIP, EIF2S2, and RALY (the ASIP-RALY gene block). After controlling for population substructure, we found that a single nucleotide polymorphism (SNP) inside the intron of RALY displays a strong pleiotropic association with cheek, crown, and breast coloration. In addition, we detect selection on the ASIP-RALY gene block, as the geographic cline of the RALY marker of this gene block has remained narrower than the plumage cline, which remained narrower than expected under neutral diffusion over two decades. Despite extensive gene flow between these species across much of the genome, the selection on ASIP-RALY gene block maintains stable genotypic and plumage difference between species allowing further differentiation to accumulate via linkage to its flanking genetic region or linkage-disequilibrium genome-wide.

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Recombination, variance in genetic relatedness, and selection against introgressed DNA

10.1101/846147 ◽

2019 ◽

Cited By ~ 2

Author(s):

Carl Veller ◽

Nathaniel B. Edelman ◽

Pavitra Muralidhar ◽

Martin A. Nowak

Keyword(s):

Gene Flow ◽

Genetic Relatedness ◽

Hybrid Vigor ◽

Recombination Rates ◽

Deleterious Alleles ◽

Genome Wide ◽

Average Proportion ◽

Positive Correlations ◽

Genomic Regions ◽

Hybrid Cross

AbstractThe genomic proportion that two relatives share identically by descent—their genetic relatedness—can vary depending on the patterns of recombination and segregation in their pedigree. Here, we calculate the precise connection between genome-wide genetic shuffling and variance in genetic relatedness. For the relationships of grandparent-grandoffspring and siblings, the variance in genetic relatedness is a simple decreasing function of , the average proportion of locus pairs that recombine in gametogenesis. These formulations explain several recent observations about variance in genetic relatedness. They further allow us to calculate the neutral variance of ancestry among F2s in a hybrid cross, enabling F2-based tests for various kinds of selection, such as Dobzhansky-Muller incompatibilities and hybrid vigor. Our calculations also allow us to characterize how recombination affects the rate at which selection eliminates deleterious introgressed DNA after hybridization—by modulating the variance of introgressed ancestry across individuals. Species with low aggregate recombination rates, like Drosophila, purge introgressed DNA more rapidly and more completely than species with high aggregate recombination rates, like humans. These conclusions also hold for different genomic regions. Within the genomes of several species, positive correlations have been observed between local recombination rate and introgressed ancestry. Our results imply that these correlations can be driven more by recombination’s effect on the purging of deleterious introgressed alleles than its effect in unlinking neutral introgressed alleles from deleterious alleles. In general, our results demonstrate that the aggregate recombination process—as quantified by and analogs—acts as a variable barrier to gene flow between species.

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The Pleistocene species pump past its prime: evidence from European butterfly sister species

10.1101/2020.09.04.282962 ◽

2020 ◽

Cited By ~ 1

Author(s):

Sam Ebdon ◽

Dominik R. Laetsch ◽

Leonardo Dapporto ◽

Alexander Hayward ◽

Michael G. Ritchie ◽

...

Keyword(s):

Gene Flow ◽

Contact Zone ◽

Sister Species ◽

Transcriptome Data ◽

Last Interglacial ◽

Species Divergence ◽

Glacial Cycles ◽

Contact Zones ◽

Genome Wide ◽

Species Pairs

AbstractThe Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. Whilst it is clear that the contact zones that have been described for many sister taxa are secondary and have formed during the last interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the embryonic stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact-zone pairs. This suggests a possible role of selective sweeps affecting mitochondrial variation in maintaining contact zones.Impact SummaryThe influence of the Pleistocene glacial cycles on structuring species and genetic diversity in temperate taxa has permeated biogeographic and phylogeographic thinking for decades. Although phylogeographic studies have repeatedly claimed that the Pleistocene acted as a species pump, systematic tests of this idea based on robust estimates of species divergence are lacking. Here we estimate divergence times for all sister species pairs of European butterfly using genome-wide transcriptome data. We find that most species pairs are substantially older than the onset of Pleistocene glacial cycling. We also show that post divergence gene flow is restricted to pairs that form contact-zones. However, in contrast to expectations under a null model of allopatric speciation contract zone pairs are not necessarily younger than sympatric pairs.

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Selection and gene flow define polygenic barriers between incipient butterfly species

10.1101/2020.04.09.034470 ◽

2020 ◽

Author(s):

Steven M. Van Belleghem ◽

Jared M. Cole ◽

Gabriela Montejo-Kovacevich ◽

Caroline N. Bacquet ◽

W. Owen McMillan ◽

...

Keyword(s):

Gene Flow ◽

Recombination Rate ◽

Genomic Variation ◽

Species Boundaries ◽

Secondary Contact ◽

Butterfly Species ◽

Demographic Modeling ◽

Incipient Species ◽

Genome Wide ◽

Genomic Divergence

AbstractCharacterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.

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Natural variation in fertility is correlated with species-wide levels of divergence inCaenorhabditis elegans

10.1101/2021.02.18.431866 ◽

2021 ◽

Author(s):

Gaotian Zhang ◽

Jake D. Mostad ◽

Erik C. Andersen

Keyword(s):

Life History ◽

Life History Traits ◽

Life History Trait ◽

Selective Sweeps ◽

C Elegans ◽

Genome Wide ◽

Fertility Variation ◽

The Face ◽

Fertility Data ◽

Genomic Regions

ABSTRACTLife history traits underlie the fitness of organisms and are under strong natural selection in the face of environmental challenges. A new mutation that positively impacts a life history trait will likely increase in frequency and become fixed in a population (e.g.selective sweep). The identification of the beneficial alleles that underlie selective sweeps provides insights into the mechanisms that occurred during the evolution of species. In the global population ofCaenorhabditis elegans,we previously identified selective sweeps that have drastically reduced chromosomal-scale genetic diversity in the species. Here, we measured the fertility (viable offspring) of a collection of wildC. elegansstrains, including many recently isolated divergent strains from the Hawaiian islands and found that strains with larger swept genomic regions on multiple chromosomes have significantly higher fertility than strains that do not have evidence of the recent selective sweeps. We used genome-wide association (GWA) mapping to identify three quantitative trait loci (QTL) underlying the fertility variation. Additionally, we mapped previous fertility data of wildC. elegansstrains andC. elegansrecombinant inbred advanced intercross lines (RIAILs) that were grown in various conditions and detected eight QTL across the genome using GWA and linkage mappings. These QTL show the genetic complexity of life history traits such as fertility across this species. Moreover, the haplotype structure in each GWA QTL region revealed correlations with recent selective sweeps in theC. eleganspopulation. North American and European strains had significantly higher fertility than most strains from Hawaii, a hypothesized origin of theC. elegansspecies, suggesting that beneficial alleles that cause increased fertility could underlie the selective sweeps during the worldwide expansion ofC. elegans.

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Global drivers of diversification in a marine species complex

10.1101/2019.12.13.874883 ◽

2019 ◽

Author(s):

Catarina N.S. Silva ◽

Nicholas P. Murphy ◽

James J. Bell ◽

Bridget S. Green ◽

Guy Duhamel ◽

...

Keyword(s):

Gene Flow ◽

Genetic Differentiation ◽

Continental Shelf ◽

Demographic History ◽

Significant Proportion ◽

Secondary Contact ◽

Larval Duration ◽

Genome Wide ◽

Extant Species ◽

Species Pairs

AbstractInvestigating historical gene flow in species complexes can indicate how environmental and reproductive barriers shape genome divergence before speciation. The processes influencing species diversification under environmental change remain one of the central focal points of evolutionary biology, particularly for marine organisms with high dispersal potential. We investigated genome-wide divergence, introgression patterns and inferred demographic history between species pairs of all extant rock lobster species (Jasus spp.), a complex with long larval duration, that has populated continental shelf and seamount habitats around the globe at approximately 40°S. Genetic differentiation patterns revealed the effects of the environment and geographic isolation. Species associated with the same habitat structure (either continental shelf or seamount/island) shared a common ancestry, even though the habitats were not adjacent. Differences in benthic temperature explained a significant proportion (41.3%) of the genetic differentiation. The Eastern Pacific species pair of J. caveorum and J. frontalis retained a signal of strict isolation following ancient migration, whereas species pairs from Australia and Africa and seamounts in the Indian and Atlantic oceans included events of introgression after secondary contact. Parameters estimated for time in isolation and gene flow were congruent with genetic differentiation metrics suggesting that the observed differentiation patterns are the product of migration and genetic drift. Our results reveal important effects of habitat and demographic processes on the divergence of species within the genus Jasus providing the first empirical study of genome-wide drivers of diversification that incorporates all extant species in a marine genus with long pelagic larval duration.

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