Clinal genomic analysis reveals strong reproductive isolation across a steep habitat transition in stickleback fish.
Ontology highlight
ABSTRACT:
SUBMITTER: Haenel Q
PROVIDER: S-EPMC8358029 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Ecological speciation seems to occur readily but is clearly not ubiquitous - and the relative contributions of different reproductive barriers remain unclear in most systems. We here investigate the potential importance of selection against migrants in lake/stream stickleback (Gasterosteus aculeatus) from the Misty Lake system, Canada. This system is of particular interest because one population contrast (Lake vs. Outlet stream) shows very low genetic and morphological divergence, whereas another population contrast (Lake vs. Inlet stream) shows dramatic genetic and morphological divergence apparently without strong and symmetric reproductive barriers. To test whether selection against migrants might solve this "conundrum of missing reproductive isolation", we performed a fully factorial reciprocal transplant experiment using 225 individually marked stickleback collected from the wild. Relative fitness of the different ecotypes (Lake, Inlet, and Outlet) was assessed based on survival and mass change in experimental enclosures. We found that Inlet fish performed poorly in the lake (selection against migrants in that direction), whereas Lake fish outperformed Inlet fish in all environments (no selection against migrants in the opposite direction). As predicted from their phenotypic and genetic similarity, Outlet and Lake fish performed similarly in all environments. These results suggest that selection against migrants is asymmetric and, together with previous work, indicates that multiple reproductive barriers contribute to reproductive isolation. Similar mosaic patterns of reproductive isolation are likely in other natural systems.
| S-EPMC3997330 | biostudies-literature
Project description:Behavioral barriers to gene flow often evolve faster than intrinsic incompatibilities and can eliminate the opportunity for hybridization between interfertile species. While acoustic signal divergence is a common driver of premating isolation in birds and insects, its contribution to speciation in mammals is less studied. Here we characterize the incidence of, and potential barriers to, hybridization among three closely related species of grasshopper mice (genus Onychomys). All three species use long-distance acoustic signals to attract and localize mates; Onychomys arenicola and Onychomys torridus are acoustically similar and morphologically cryptic whereas Onychomys leucogaster is larger and acoustically distinct. We used genotyping-by-sequencing (GBS) to test for evidence of introgression in 227 mice from allopatric and sympatric localities in the western United States and northern Mexico. We conducted laboratory mating trials for all species pairs to assess reproductive compatibility, and recorded vocalizations from O. arenicola and O. torridus in sympatry and allopatry to test for evidence of acoustic character displacement. Hybridization was rare in nature and, contrary to prior evidence for O. torridus/O. arenicola hybrids, only involved O. leucogaster and O. arenicola. In contrast, laboratory crosses between O. torridus and O. arenicola produced litters whereas O. leucogaster and O. arenicola crosses did not. Call fundamental frequency in O. torridus and O. arenicola was indistinguishable in allopatry but significantly differentiated in sympatry, a pattern consistent with reproductive character displacement. These results suggest that assortative mating based on a long-distance signal is an important isolating mechanism between O. torridus and O. arenicola and highlight the importance of behavioral barriers in determining the permeability of species boundaries.
| S-EPMC6875671 | biostudies-literature
Project description:The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.
| S-EPMC7423277 | biostudies-literature
Project description:We possess limited understanding of how speciation unfolds in the most species-rich region of the planet-the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.
| S-EPMC5879619 | biostudies-literature
Project description:Interactions between species are central to evolution and ecology, but we do not know enough about how outcomes of interactions between species vary across geographic locations, in heterogeneous environments, or over time. Ecological dimensions of interactions between species are known to vary, but evolutionary interactions such as the establishment and maintenance of reproductive isolation are often assumed to be consistent across instances of an interaction between species. Hybridization among Catostomus fish species occurs over a large and heterogeneous geographic area and across taxa with distinct evolutionary histories, which allows us to assess consistency in species interactions. We analyzed hybridization among six Catostomus species across the Upper Colorado River basin (US mountain west) and found extreme variation in hybridization across locations. Different hybrid crosses were present in different locations, despite similar species assemblages. Within hybrid crosses, hybridization varied from only first generation hybrids to extensive hybridization with backcrossing. Variation in hybridization outcomes might result from uneven fitness of hybrids across locations, polymorphism in genetic incompatibilities, chance, unidentified historical contingencies, or some combination thereof. Our results suggest caution in assuming that one or a few instances of hybridization represent all interactions between the focal species, as species interactions vary substantially across locations.
| S-EPMC6121845 | biostudies-other
Project description:How rapidly natural selection sorts genome-wide standing genetic variation during adaptation remains largely unstudied experimentally. Here, we present a genomic release-recapture experiment using paired threespine stickleback fish populations adapted to selectively different lake and stream habitats. First, we use pooled whole-genome sequence data from the original populations to identify hundreds of candidate genome regions likely under divergent selection between these habitats. Next, we generate F2 hybrids from the same lake-stream population pair in the laboratory and release thousands of juveniles into a natural stream habitat. Comparing the individuals surviving one year of stream selection to a reference sample of F2 hybrids allows us to detect frequency shifts across the candidate regions toward the genetic variants typical of the stream population-an experimental outcome consistent with polygenic directional selection. Our study reveals that adaptation in nature can be detected as a genome-wide signal over just a single generation.
| S-EPMC7174299 | biostudies-literature
Project description:Recent studies have revealed that 2-3% of the genome of non-Africans might come from Neanderthals, suggesting a more complex scenario of modern human evolution than previously anticipated. In this paper, we use a model of admixture during a spatial expansion to study the hybridization of Neanderthals with modern humans during their spread out of Africa. We find that observed low levels of Neanderthal ancestry in Eurasians are compatible with a very low rate of interbreeding (<2%), potentially attributable to a very strong avoidance of interspecific matings, a low fitness of hybrids, or both. These results suggesting the presence of very effective barriers to gene flow between the two species are robust to uncertainties about the exact demography of the Paleolithic populations, and they are also found to be compatible with the observed lack of mtDNA introgression. Our model additionally suggests that similarly low levels of introgression in Europe and Asia may result from distinct admixture events having occurred beyond the Middle East, after the split of Europeans and Asians. This hypothesis could be tested because it predicts that different components of Neanderthal ancestry should be present in Europeans and in Asians.
| S-EPMC3174651 | biostudies-literature
Project description:Large structural variations (SVs) within genomes are more challenging to identify than smaller genetic variants but may substantially contribute to phenotypic diversity and evolution. We analyse the effects of SVs on gene expression, quantitative traits and intrinsic reproductive isolation in the yeast Schizosaccharomyces pombe. We establish a high-quality curated catalogue of SVs in the genomes of a worldwide library of S. pombe strains, including duplications, deletions, inversions and translocations. We show that copy number variants (CNVs) show a variety of genetic signals consistent with rapid turnover. These transient CNVs produce stoichiometric effects on gene expression both within and outside the duplicated regions. CNVs make substantial contributions to quantitative traits, most notably intracellular amino acid concentrations, growth under stress and sugar utilization in winemaking, whereas rearrangements are strongly associated with reproductive isolation. Collectively, these findings have broad implications for evolution and for our understanding of quantitative traits including complex human diseases.
| S-EPMC5286201 | biostudies-literature
Project description:Background and aimsThe events leading to speciation are best investigated in systems where speciation is ongoing or incomplete, such as incipient species. By examining reproductive barriers among incipient sister taxa and their congeners we can gain valuable insights into the relative timing and importance of the various barriers involved in the speciation process. The aim of this study was to identify the reproductive barriers among sexually deceptive orchid taxa in the genus Chiloglottis.MethodsThe study targeted four closely related taxa with varying degrees of geographic overlap. Chemical, morphological and genetic evidence was combined to explore the basis of reproductive isolation. Of primary interest was the degree of genetic differentiation among taxa at both nuclear and chloroplast DNA markers. To objectively test whether or not species boundaries are defined by the chemistry that controls pollinator specificity, genetic analysis was restricted to samples of known odour chemistry.Key resultsFloral odour chemical analysis was performed for 600+ flowers. The three sympatric taxa were defined by their specific chiloglottones, the semiochemicals responsible for pollinator attraction, and were found to be fully cross-compatible. Multivariate morphometric analysis could not reliably distinguish among the four taxa. Although varying from very low to moderate, significant levels of genetic differentiation were detected among all pairwise combinations of taxa at both nuclear and chloroplast loci. However, the levels of genetic differentiation were lower than expected for mature species. Critically, a lack of chloroplast DNA haplotype sharing among the morphologically indistinguishable and most closely related taxon pair confirmed that chemistry alone can define taxon boundaries.ConclusionsThe results confirmed that pollinator isolation, mediated by specific pollinator attraction, underpins strong reproductive isolation in these taxa. A combination of large effective population sizes, initial neutral mutations in the genes controlling floral scent, and a pool of available pollinators likely drives diversity in this system.
| S-EPMC3890385 | biostudies-literature
Project description:Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, especially in regards to highly vulnerable marine ecosystems. In this context, cryptic species are particularly challenging to conserve because they are hard to distinguish based on morphology alone, and thus it is often unclear how many species coexist in sympatry, what are their phylogenetic relationships and their demographic history. We answer these questions using morphologically similar species of the genus Mugil that are sympatric in the largest coastal Marine Protected Area in the Tropical Southwestern Atlantic marine province. Using a sub-representation of the genome, we show that individuals are assigned to five highly differentiated genetic clusters that are coincident with five mitochondrial lineages, but discordant with morphological information, supporting the existence of five species with conserved morphology in this region. A lack of admixed individuals is consistent with strong genetic isolation between sympatric species, but the most likely species tree suggests that in one case speciation has occurred in the presence of interspecific gene flow. Patterns of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions since species formation. Together, our results show that strong morphologic conservatism in marine environments can lead to species that are difficult to distinguish morphologically but that are characterized by an independent evolutionary history, and thus that deserve species-specific management strategies.
| S-EPMC8405619 | biostudies-literature