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

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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Biodiversity genomics of North American Dryobates woodpeckers reveals little gene flow across the D. nuttallii x D. scalaris contact zone

The Auk ◽

10.1093/auk/ukz015 ◽

2019 ◽

Vol 136 (2) ◽

Author(s):

Joseph D Manthey ◽

Stéphane Boissinot ◽

Robert G Moyle

Keyword(s):

Gene Flow ◽

Contact Zone ◽

Genomic Diversity ◽

Whole Genome ◽

Effective Population ◽

Contact Zones ◽

Population Sizes ◽

Speciation Continuum ◽

Whole Genome Resequencing ◽

Genomic Introgression

Abstract Evolutionary biologists have long used behavioral, ecological, and genetic data from contact zones between closely related species to study various phases of the speciation continuum. North America has several concentrations of avian contact zones, where multiple pairs of sister lineages meet, with or without hybridization. In a southern California contact zone, 2 species of woodpeckers, Nuttall’s Woodpecker (Dryobates nuttallii) and the Ladder-backed Woodpecker (D. scalaris), occasionally hybridize. We sampled these 2 species in a transect across this contact zone and included samples of their closest relative, the Downy Woodpecker (D. pubescens), to obtain large single nucleotide polymorphism panels using restriction-site associated DNA sequencing (RAD-seq). Furthermore, we used whole-genome resequencing data for 2 individuals per species to identify whether patterns of diversity inferred from RAD-seq were representative of whole-genome diversity. We found that these 3 woodpecker species are genomically distinct. Although low levels of gene flow occur between D. nuttallii and D. scalaris across the contact zone, there was no evidence for widespread genomic introgression between these 2 species. Overall patterns of genomic diversity from the RAD-seq and wholegenome datasets appear to be related to distributional range size and, by extension, are likely related to effective population sizes for each species.

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Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

10.1101/2020.09.08.287151 ◽

2020 ◽

Cited By ~ 1

Author(s):

Thomas C. Nelson ◽

Angela M. Stathos ◽

Daniel D. Vanderpool ◽

Findley R. Finseth ◽

Yao-wu Yuan ◽

...

Keyword(s):

Gene Flow ◽

Evolutionary History ◽

Species Tree ◽

Sister Species ◽

Pollination Syndrome ◽

Gene Trees ◽

Trait Evolution ◽

Genome Wide ◽

Hummingbird Pollination ◽

History Of

AbstractInferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.

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Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.2630 ◽

2018 ◽

Vol 285 (1871) ◽

pp. 20172630 ◽

Cited By ~ 11

Author(s):

Jacco C. van Rijssel ◽

Florian N. Moser ◽

David Frei ◽

Ole Seehausen

Keyword(s):

Gene Flow ◽

Natural Selection ◽

Genetic Differentiation ◽

Lake Victoria ◽

Sister Species ◽

Disruptive Selection ◽

Nuptial Coloration ◽

Ecological Selection ◽

Evolutionary Response ◽

Species Pairs

Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence of disruptive ecological selection differs between sympatric sister species that are at different stages of speciation. Some of our species pairs do ( Pundamilia ) and others do not ( Neochromis ) differ distinctively in sexually selected male nuptial coloration. We find that (i) evidence for disruptive selection, and for evolutionary response to it, is prevalent in traits that are differentiated between sister species; (ii) prevalence of both predicts the extent of genetic differentiation; and (iii) genetic differentiation is weaker in species pairs with conserved male nuptial coloration. Our results speak to the existence of two different mechanisms of speciation with gene flow: speciation mainly by sexual selection tightly followed by ecological character displacement in some cases and speciation mainly by divergent ecological selection in others.

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

10.1101/190629 ◽

2017 ◽

Cited By ~ 1

Author(s):

Mark Ravinet ◽

Kohta Yoshida ◽

Shuji Shigenobu ◽

Atsushi Toyoda ◽

Asao Fujiyama ◽

...

Keyword(s):

Gene Flow ◽

Pacific Ocean ◽

Japan Sea ◽

Species Pair ◽

Genome Wide ◽

Species Pairs ◽

Genomic Divergence ◽

The Face ◽

Genomic Regions ◽

Japanese Islands

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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Faculty Opinions recommendation of Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.725563097.793507503 ◽

2015 ◽

Author(s):

Norman Johnson

Keyword(s):

Gene Flow ◽

Experimental Evidence ◽

Early Stages ◽

Ecological Selection ◽

Genome Wide

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Landscape resistance constrains hybridization across contact zones in a reproductively and morphologically polymorphic salamander

Scientific Reports ◽

10.1038/s41598-021-88349-7 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Guillermo Velo-Antón ◽

André Lourenço ◽

Pedro Galán ◽

Alfredo Nicieza ◽

Pedro Tarroso

Keyword(s):

Contact Zone ◽

Environmental Heterogeneity ◽

Evolutionary Dynamics ◽

Morphological Differentiation ◽

Phenotypic Traits ◽

Hybrid Zones ◽

Landscape Resistance ◽

Phenotypic Differentiation ◽

Contact Zones

AbstractExplicitly accounting for phenotypic differentiation together with environmental heterogeneity is crucial to understand the evolutionary dynamics in hybrid zones. Species showing intra-specific variation in phenotypic traits that meet across environmentally heterogeneous regions constitute excellent natural settings to study the role of phenotypic differentiation and environmental factors in shaping the spatial extent and patterns of admixture in hybrid zones. We studied three environmentally distinct contact zones where morphologically and reproductively divergent subspecies of Salamandra salamandra co-occur: the pueriparous S. s. bernardezi that is mostly parapatric to its three larviparous subspecies neighbours. We used a landscape genetics framework to: (i) characterise the spatial location and extent of each contact zone; (ii) assess patterns of introgression and hybridization between subspecies pairs; and (iii) examine the role of environmental heterogeneity in the evolutionary dynamics of hybrid zones. We found high levels of introgression between parity modes, and between distinct phenotypes, thus demonstrating the evolution to pueriparity alone or morphological differentiation do not lead to reproductive isolation between these highly divergent S. salamandra morphotypes. However, we detected substantial variation in patterns of hybridization across contact zones, being lower in the contact zone located on a topographically complex area. We highlight the importance of accounting for spatial environmental heterogeneity when studying evolutionary dynamics of hybrid zones.

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Introgression between non-sister species of honeyeaters (Aves: Meliphagidae) several million years after speciation

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz129 ◽

2019 ◽

Vol 128 (3) ◽

pp. 583-591

Author(s):

Leo Joseph ◽

Alex Drew ◽

Ian J Mason ◽

Jeffrey L Peters

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Sex Chromosomes ◽

Common Ancestor ◽

Sister Species ◽

Species Boundaries ◽

North Eastern ◽

The City

Abstract We reassessed whether two parapatric non-sister Australian honeyeater species (Aves: Meliphagidae), varied and mangrove honeyeaters (Gavicalis versicolor and G. fasciogularis, respectively), that diverged from a common ancestor c. 2.5 Mya intergrade in the Townsville area of north-eastern Queensland. Consistent with a previous specimen-based study, by using genomics methods we show one-way gene flow for autosomal but not Z-linked markers from varied into mangrove honeyeaters. Introgression barely extends south of the area of parapatry in and around the city of Townsville. While demonstrating the long-term porosity of species boundaries over several million years, our data also suggest a clear role of sex chromosomes in maintaining reproductive isolation.

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