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Rapid evolutionary divergence of a songbird population following recent colonization of an urban area
<p>Colonization of a novel environment by a small group of individuals can lead to rapid evolutionary change, yet evidence of the relative contributions of neutral and selective factors in promoting divergence during the early stages of colonization remain scarce. Here, we use genome-wide SNP data to test the role of neutral and selective forces in driving the divergence of a unique urban population of the Oregon junco (<em>Junco hyemalis oreganus</em>), which became established on the campus of the University of California at San Diego (UCSD) in the early 1980s. Previous studies based on microsatellite loci documented significant genetic differentiation of the urban population as well as divergence in sexual signaling and life-history traits relative to nearby montane populations. However, the geographic origin of the colonization and the factors involved in the onset of the differentiation process remained uncertain. Our genome-wide SNP dataset confirmed the marked genetic differentiation of the UCSD population, and phylogenomic analysis identified the coastal subspecies <em>pinosus</em> from central California as its sister group instead of the neighboring mountain population. Demographic inference based on site frequency spectra recovered a time of separation from <em>pinosus</em> as recent as 20 to 32 generations, and a strong bottleneck at the time of colonization, suggesting a relevant role of founder effects and drift in the genetic differentiation of the UCSD population. However, we also found significant associations between environmental parameters characterizing the urban habitat of UCSD and genome-wide variants linked to functional genes. Some of the identified gene functions, like heavy metal detoxification and high-pitched hearing, have been reported as potentially adaptive in birds inhabiting urban environments. These results suggest that the interplay between founder events and directional selection may result in rapid shifts in both neutral and adaptive loci across the genome, and reveal the UCSD population of juncos as an ongoing case of divergence following the colonization of an anthropic environment.</p>
Interspecific hybridization explains rapid gorget color divergence in Heliodoxa hummingbirds (Aves: Trochilidae)
Hybridization is a known source of morphological, functional, and communicative signal novelty in many organisms. Although diverse mechanisms of established novel ornamentation have been identified in natural populations, we lack an understanding of hybridization effects across levels of biological scales and upon phylogenies. Hummingbirds display diverse structural colors resulting from coherent light scattering by feather nanostructures. Given the complex relationship between feather nanostructures and the colors they produce, intermediate coloration does not necessarily imply intermediate nanostructures. Here, we characterize nanostructural, ecological, and genetic inputs in a distinctive Heliodoxa hummingbird from the foothills of eastern Peru. Genetically, this individual is closely allied with Heliodoxa branickii and H. gularis, but it is not identical to either when nuclear data are assessed. Elevated interspecific heterozygosity further suggests it is a hybrid backcross to H. branickii. Electron microscopy and spectrophotometry of this unique individual reveal key nanostructural differences underlying its distinct gorget color, confirmed by optical modeling. Phylogenetic comparative analysis suggests that the observed gorget coloration divergence from both parentals to this individual would take 6.6–10 My to evolve at the current rate within a single hummingbird lineage. These results emphasize the mosaic nature of hybridization and suggest that hybridization may contribute to the structural color diversity found across hummingbirds.
Rapid evolutionary divergence of a songbird population following recent colonization of an urban area
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Interspecific hybridization explains rapid gorget color divergence in Heliodoxa hummingbirds (Aves: Trochilidae)
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Data from: Quantitative proteomics reveals rapid divergence in the postmating response of female reproductive tracts among sibling species
<p><span><span><span><span><span><span><span><span><span><span><span>Fertility depends, in part, on interactions between male and female reproductive proteins inside the female reproductive tract (FRT) that mediate postmating changes in female behavior, morphology, and physiology. Coevolution between interacting proteins within species may drive reproductive incompatibilities between species, yet the mechanisms underlying postmating-prezygotic isolating barriers remain poorly resolved. Here, we used quantitative proteomics in sibling <i>Drosophila</i> species to investigate the molecular composition of the FRT environment and its role in mediating species-specific postmating responses. We found that (1) FRT proteomes in <i>D. simulans</i> and<i> D. mauritiana</i> virgin females express unique combinations of secreted proteins and are enriched for distinct functional categories, (2) mating induces substantial changes to the FRT proteome in <i>D. mauritiana</i> but not in <i>D. simulans</i>, and (3) the <i>D. simulans </i>FRT proteome exhibits limited postmating changes irrespective of whether females mate with conspecific or heterospecific males, suggesting an active female role in mediating reproductive interactions. Comparisons with similar data in the closely related outgroup species <i>D. melanogaster </i>suggest that divergence is concentrated on the <i>D. simulans </i>lineage. Our study suggests that divergence in the FRT extracellular environment and postmating response contribute to previously described patterns of postmating-prezygotic isolation and the maintenance of species boundaries.</span></span></span></span></span></span></span></span></span></span></span></p>
Data from: Repeated divergence in opsin genes expression mirrors photic habitat changes in rapidly evolving crater lake cichlid fishes
<div> <div> <div class="msocomtxt"> <p class="MsoNormal"><span>Selection pressures differ along environmental gradients and organisms' phenotypes. Traits tightly linked to fitness (e.g., the visual system) are expected to closely track environmental variation along gradients. Within such gradients, adaptation to local conditions might be due to heritable and non-heritable, environmentally induced variation. Disentangling these sources of phenotypic variation requires studying, in nature and the laboratory, closely related populations experiencing different environments. The Nicaraguan great and crater lakes show an environmental gradient in photic conditions extending from clear crater lakes to very turbid great lakes. From two old, turbid great lakes, Midas cichlid fish (<em>Amphilophus </em>cf.<em> citrinellus</em>) independently colonized seven isolated crater lakes of varying light conditions, resulting in a small adaptive radiation. We estimated the variation in visual sensitivities along this photic gradient by measuring differential cone opsin gene expression among populations from different lakes. The visual sensitivities observed in all seven derived crater lake populations have not changed randomly but shifted predictably in direction and magnitude, repeatedly mirroring changes in photic conditions. Intrapopulation phenotypic variation decreases as environments become spectrally narrower suggesting different selective landscapes within the gradient. Comparing wild-caught and lab-reared fish revealed that 48% of this phenotypic variation is genetically determined and evolved rapidly. Our results demonstrate deterministic, rapid phenotypic evolution that fine-tunes visual sensitivity to fine-scale environmental variation.</span></p> <p class="MsoCommentText"><span> </span></p> </div> </div> </div>
Rapid divergent evolution of internal female genitalia and the coevolution of male genital morphology revealed by micro-computed tomography
<p>Animal genitalia are thought to evolve rapidly and divergently in response to sexual selection. Studies of genital evolution have focused largely on male genitalia, with our understanding of female genital evolution relatively limited. The paucity of work on female genital morphology is likely due to problems faced in quantifying shape variation, due to their composition and accessibility. Here we use a combination of micro-computed tomography, landmark-free shape quantification, and phylogenetic analysis to quantify the rate of female genital shape evolution among 29 species of Antichiropus millipedes, and the coevolution of male genitalia. We found significant variation in female and male genital shape among species. While male genital shape showed significant phylogenetic signal, female genital shape did not. Male genital shape was found to be evolving 1.2 times faster than female genital shape. Female and male genital shapes exhibited strongly correlated evolution, indicating that genital shape changes in one sex are associated with corresponding changes in the genital shape of the other sex. This study adds novel insight into our growing understanding of how female genitalia can evolve rapidly and divergently and highlights the advantages of three-dimensional techniques and multivariate analyses in studies of female genital evolution.</p>
Habitat fragmentation induces rapid phenotypic divergence of migratory and isolated sticklebacks
<p>The adaptive capacity of many organisms is seriously challenged by human-imposed environmental change, which currently happens at unprecedented rates and magnitudes. For migratory fish, habitat fragmentation is a major challenge that can compromise their survival and reproduction. Therefore, it is important to study if fish populations can adapt to such modifications of their habitat. Here, we study whether originally anadromous three-spined stickleback populations (Gasterosteus aculeatus; 'migrants') changed in behavior and morphology in response to human-induced isolation. We made use of a natural field-experiment, where the construction of pumping stations and sluices in the 1970s unintendedly created replicates of land-locked stickleback populations ('resident') in the Netherlands. For two years, we systematically tested populations of residents and migrants for differences in morphology and behavioral traits (activity, aggressiveness, exploration, boldness and shoaling) in lab-based assays. We detected differences between migrant and resident populations in virtually all phenotypic traits studied: compared to the ancestral migrants, residents were smaller in size, had fewer and smaller plates and were significantly more active, aggressive, exploratory and bolder and shoaled less. Despite large ecological differences between 2018 and 2019, results were largely consistent across the two years. Our study shows that human-induced environmental change has led to the rapid and consistent morphological and behavioral divergence of stickleback populations in about 50 generations. Such changes may be adaptive but this remains to be tested.</p>
Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
Y chromosomes across diverse species convergently evolve a gene-poor, heterochromatic organization enriched for duplicated genes, LTR retrotransposons, and satellite DNA. Sexual antagonism and a loss of recombination play major roles in the degeneration of young Y chromosomes. However, the processes shaping the evolution of mature, already degenerated Y chromosomes are less well-understood. Because Y chromosomes evolve rapidly, comparisons between closely related species are particularly useful. We generated de novo long read assemblies complemented with cytological validation to reveal Y chromosome organization in three closely related species of the Drosophila simulans complex, which diverged only 250,000 years ago and share >98% sequence identity. We find these Y chromosomes are divergent in their organization and repetitive DNA composition and discover new Y-linked gene families whose evolution is driven by both positive selection and gene conversion. These Y chromosomes are also enriched for large deletions, suggesting that the repair of double-strand breaks on Y chromosomes may be biased toward microhomology-mediated end joining over canonical non-homologous end-joining. We propose that this repair mechanism contributes to the convergent evolution of Y chromosome organization across organisms.
Demographic modelling helps tracking the rapid and recent divergence of a conifer species pair from central Mexico
<p>Secondary contact of recently diverged species may have several outcomes, ranging from rampant hybridization to reinforced reproductive isolation. In plants, selfing tolerance and disjunct reproductive phenology may lead to reproductive isolation at contact zones. However, they can evolve under both allopatric or parapatric frameworks and originate from adaptive and/or neutral forces. Inferring the historical demography of diverging taxa is thus a crucial step to identify those factors that may lead to putative reproductive isolation. We explored various competing hypotheses to account for the rapid divergence of a fir species complex (<em>Abies flinckii - A. religiosa</em>) distributed in 'sky-islands' across central Mexico (i.e., along the Trans-Mexican Volcanic Belt; TMVB). Despite co-occurring in two independent sympatric regions (west and center), these taxa rarely interbreed because of disjunct reproductive phenologies. We genotyped 1,147 SNPs, generated by GBS, across 23 populations, and compared multiple demographic scenarios based on the geological history of the TMVB. The best-fitting model revealed one of the most rapid and complete speciation cases for a conifer species-pair, dating back to ~1.2 Ma. Coupled with the lack of support for stepwise colonization, our coalescent inferences point to an early cessation of interspecific gene flow under parapatric speciation; ancestral gene flow during divergence was asymmetrical (mostly from western firs into A. religiosa) and exclusive to the most ancient (i.e., central) contact zone. Factors promoting rapid reproductive isolation should be explored in other slowly-evolving species complexes as they may account for the large tropical and subtropical diversity.</p>
Target capture methods offer insight into the evolution of rapidly diverged taxa and resolve allopolyploid homeologs in the fern genus Polypodium s.s.
<p><span></span></p> <p>Like many fern lineages comprising reticulate species complexes, <em>Polypodium</em> s.s. (Polypodiacaeae) has a history shaped by rapid diversification, hybridization, and polyploidy that poses substantial challenges for phylogenetic inference with plastid and single-locus nuclear loci. Using target capture probes for 408 nuclear loci developed by the GOFlag project and a custom bioinformatic pipeline, SORTER, we constructed multi-locus nuclear datasets for diploid temperate and Mesoamerican species of <em>Polypodium</em> and five allotetraploid species belonging to the well-studied <em>Polypodium</em> <em>vulgare</em> complex. SORTER employs a clustering approach to separate putatively paralogous copies of targeted loci into orthologous matrices and haplotype phasing to infer allopolyploid haplotypes across loci, resulting in datasets amenable to both concatenated maximum likelihood and multi-species coalescent phylogenetic analyses. By comparing phylogenies derived from maximum likelihood and multi- species coalescent analyses of unphased and phased datasets, as well as evaluating discordance among gene trees and species trees, we recover support for incomplete lineage sorting within <em>Polypodium</em> s.s., novel relationships among diploid taxa of the <em>Polypodium</em> <em>vulgare</em> complex and its Mesoamerican sister clade, and the placement of several <em>Polypodium</em> species within other genera. Additionally, we were able to infer well-supported phylogenies that identified the hypothesized progenitors of the allotetraploid species, indicating that SORTER is an effective and accurate tool for reconstructing homeolog haplotypes of allopolyploids in fern taxa and other non-model organisms from target capture data.</p>
Data from: Experimental evolution of halophiles: rapid divergence along a multidimensional niche
<p>This data was collected during the study entitled "Experimental evolution of halophiles: rapid divergence along a multidimensional niche."</p> <p>We explored multidimensional niche breadth evolution among two halophilic species, an archaeon (<em>Halobacterium salinarum</em>) and a bacterium (<em>Salinibacter ruber</em>). We propagated each species in rich and poor media for 60 generations and measured associated changes across novel conditions. In particular, we isolated the effects of selection history on axes of salinity and resource abundance, documenting whether shifts in niche breadth are context-dependent.</p> <p>Growth curves were generated via daily measurements over 5 days (4 replicate populations per treatment), with the area under the curve used as a proxy for absolute fitness in a given environment. Relative fitness was calculated as the fitness of the derived populations (following 10 transfers in their respective environment) divided by the fitness of the ancestral populations. </p>
Genomic signatures of rapid adaptive divergence in a tropical montane species
<p>This dataset contains data from a study described in the paper: Ericson, P.G.P., Irestedt, M., She, H., and Qu, Y. (2021) "Genomic signatures of rapid adaptive divergence in a tropical montane species". <em>Biology Letters</em> (in print).</p> <p>The study investigates allopatric divergence and selection in Archbold's Bowerbird (<i>Amblyornis papuensis</i>), an iconic bird living in a tropical mountain region in New Guinea, using a novel chromosome-level genome and population genomic comparisons.</p> <p>Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11,800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is likely associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between eastern and western Central Range likely drive adaptive divergence between them.</p>
Rapid divergent evolution of an annual plant across a latitudinal gradient revealed by seed resurrection
<p>Global change is expected to drive short-term evolution of natural populations. However, it remains unclear whether different populations are changing in unison. Here, we study contemporary evolution of growth-related and reproductive traits of three populations of <i>Cyanus segetum</i> face to warming and pollinator decline across a latitudinal gradient in France. We resurrected stored seeds sampled up to 24 years apart from northern, central-western, and southern populations and conducted an <i>in situ</i> common-garden experiment. To disentangle neutral from selection-driven differentiation, we calculated neutral genetic differentiation (<i>F<sub>ST</sub></i>) and quantitative trait differentiation (<i>Q<sub>ST</sub></i>) between temporal samples. We found that phenotypic evolution was divergent across populations exhibiting different trends for rosette size, date of flowering, and capitula size. By measuring seed set as a proxy of fitness, we showed that samples with larger mean capitula size outperformed samples with smaller mean capitula size in the western and southern populations. Regression of traits on seed set showed that flowering date and capitula size are the primary determinants of fitness, and <i>Q<sub>ST</sub>-F<sub>S</sub></i><i><sub>T</sub></i> comparisons indicated that natural selection has likely contributed to the shifts in flowering phenology and rosette size. These findings outline the potential for rescue of natural populations through contemporary evolution and emphasize the complex interplay between spatial and temporal variation in species' responses to global change.</p>
The role of sexual isolation during rapid ecological divergence: evidence for a new dimension of isolation in Rhagoletis pomonella
<p>The pace of divergence and likelihood of complete speciation may depend on how and when different types of reproductive barriers evolve. Questions remain about the evolution of reproductive barriers after initial divergence. We tested for the presence of sexual isolation (reduced mating between populations due to divergent mating preferences and traits) in <em>Rhagoletis</em> <em>pomonella</em> flies, a model system for incipient ecological speciation. We measured the strength of sexual isolation between two very recently diverged (~170 generations) sympatric populations, adapted to different host fruits (hawthorn and apple). We found that flies from both populations were more likely to mate within than between populations. Thus, sexual isolation may play an important role in reducing gene flow allowed by early-acting ecological barriers. We also tested how warmer temperatures predicted under climate change could alter sexual isolation and found that sexual isolation was markedly asymmetric under warmer temperatures – apple males and hawthorn females mated randomly while apple females and hawthorn males mated within population than between. Our findings provide a window into the early divergence process and the role of sexual isolation after initial ecological divergence, in addition to examining how environmental conditions could shape the likelihood of further divergence.</p>
Rapid sperm length divergence in a polygynandrous passerine: a mechanism of cryptic speciation?
<p>When populations become geographically isolated, they begin to diverge in various traits and at variable rates. The dynamics of such trait divergences are relevant for understanding evolutionary processes such as local adaptation and speciation. Here we examine divergences in sperm and body structures in a polygynandrous songbird, the alpine accentor (<em>Prunella</em> <em>collaris</em>) between two allopatric high-altitude populations, in Morocco and Spain. The populations diverged around 82,000 years ago, as estimated with a coalescence-based phylogenetic analysis of genome-wide single nucleotide polymorphisms. We found that birds in the two areas had non-overlapping sperm lengths. This suggests adaptation to divergent female reproductive tract environments. Sperm length also showed an exceptionally low coefficient of among-male variation, a signal of strong stabilizing selection imposed by sperm competition. The evolutionary rate of sperm length was almost twice the rates for the most divergent morphological traits, and more than three times higher than expected from literature data over a similar generational timescale. This rapid evolution of a key reproductive trait has implications for reproductive isolation and ultimately for speciation. Strong selection for different sperm length optima in allopatry predicts conspecific sperm precedence and disruptive selection in sympatry, hence a possible postcopulatory prezygotic barrier to gene flow.</p>
Demographic modelling helps tracking the rapid and recent divergence of a conifer species pair from central Mexico
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Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
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Target capture methods offer insight into the evolution of rapidly diverged taxa and resolve allopolyploid homeologs in the fern genus Polypodium s.s.
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Genomic signatures of rapid adaptive divergence in a tropical montane species
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