Evolution of assortative mating following selective introgression of pigmentation genes between two Drosophila species

Adaptive introgression is ubiquitous in animals but experimental support for its role in driving speciation remains scarce. In the absence of conscious selection, admixed laboratory strains of Drosophila asymmetrically and progressively lose alleles from one parental species and reproductive isolation against the predominant parent ceases after 10 generations. Here, we selectively introgressed during one year light pigmentation genes of D. santomea into the genome of its dark sibling D. yakuba, and vice versa. We found that the pace of phenotypic change differed between the species and the sexes, and identified through genome sequencing common as well as distinct introgressed loci in each species. Mating assays showed that assortative mating between introgressed flies and both parental species persisted even after four years (~ 60 generations) from the end of the selection. Those results indicate that selective introgression of as low as 0.5% of the genome can beget morphologically-distinct and reproductively-isolated strains, two prerequisites for the delimitation of new species. Our findings hence represent a significant step towards understanding the genome-wide dynamics of speciation-through-introgression.

Population genomic evidence of selection on structural variants in a natural hybrid zone

Structural variants (SVs) can promote speciation by directly causing reproductive isolation or by suppressing recombination across large genomic regions. Whereas examples of each mechanism have been documented, systematic tests of the role of SVs in speciation are lacking. Here, we take advantage of long-read (Oxford nanopore) whole-genome sequencing and a hybrid zone between two Lycaeides butterfly taxa (L. melissa and Jackson Hole Lycaeides) to comprehensively evaluate genome-wide patterns of introgression for SVs and relate these patterns to hypotheses about speciation. We found >100,000 SVs segregating within or between the two hybridizing species. SVs and SNPs exhibited similar levels of genetic differentiation between species, with the exception of inversions, which were more differentiated. We detected credible variation in patterns of introgression among SV loci in the hybrid zone, with 562 of 1419 ancestry-informative SVs exhibiting genomic clines that deviating from null expectations based on genome-average ancestry. Overall, hybrids exhibited a directional shift towards Jackson Hole Lycaeides ancestry at SV loci, consistent with the hypothesis that these loci experienced more selection on average then SNP loci. Surprisingly, we found that deletions, rather than inversions, showed the highest skew towards excess introgression from Jackson Hole Lycaeides. Excess Jackson Hole Lycaeides ancestry in hybrids was also especially pronounced for Z-linked SVs and inversions containing many genes. In conclusion, our results show that SVs are ubiquitous and suggest that SVs in general, but especially deletions, might contribute disproportionately to hybrid fitness and thus (partial) reproductive isolation.

Speciation in the Cladophorales species flock of ancient Lake Baikal

<p>Understanding speciation is one of the great challenges in evolutionary biology as many of the processes involved in speciation, as well as the forces leading to morphological and genetic differentiation, are not fully understood. Three main modes of speciation have been described: allopatric, parapatric and sympatric. Sympatric speciation is the most enigmatic mode because in the absence of physical barriers, disruptive selection, assortative mating and hybridization play central roles in reproductive isolation. Although it is accepted that sympatric speciation is possible, only a few examples of this process exist to date. Another common method of speciation in plants and algae is via polyploidization. Recently, a promising system to study speciation in sympatry was discovered: the endemic Cladophorales species flock in ancient Lake Baikal, Russia. The flock consists of sixteen taxa grouped in four genera: Chaetocladiella, Chaetomorpha, Cladophora and Gemmiphora. In spite of their morphological diversity, recent molecular analyses have shown that this is a monophyletic group with low genetic variation and nested within the morphologically simple genus Rhizoclonium. Due to their high number of species, endemism and sympatric distribution, many interesting questions have arisen such as what processes are involved in speciation, and whether this group might be a novel example of sympatric speciation. In this study, we analysed the population genetics of the endemic Baikalian Cladophorales to infer the processes shaping the evolution of the group. First, a set of microsatellites was designed using high-throughput sequencing data. Second, species delimitation methods based on genetic clustering were performed. Third, the population genetics of three widely distributed species was analysed looking for evidence of panmixia, a common criteria to support sympatric speciation. A total of 11 microsatellites that mostly cross-amplify between most species were obtained. The genotyping revealed that most loci had more than two alleles per individual indicating polyploidy. As such, the analyses required a different approach which consisted in coding the genotypes as ‘allelic phenotypes’, allowing the use of individuals of different ploidy levels in the same data set. The species delimitation of 15 operative morphotaxa and 727 individuals supported reproductive isolation of five morphotaxa and two hypotheses of conspecificity. However, some morphotaxa showed unclear assignments revealing the need of further research to clarify their reproductive limits. Finally, the population genetics of Chaetomorpha moniliformis, Cladophora compacta and Cl. kursanovii revealed patterns of genetic variation and structure that suggest different reproductive strategies and dispersal abilities. This demonstrates that contrasting biological characteristics may arise in closely related lineages: Chaetomorpha moniliformis with dominant asexual reproduction and long dispersal abilities; Cladophora compacta with high genetic diversity, no population structure and likely to reproduce sexually; Cl. kursanovii with a structure congruent with geographic distribution and more restricted dispersal. The results suggest that polyploidy, rather than speciation with gene flow, is the force driving the reproductive isolation and evolution of this flock. Although many questions remain to be studied, this research provides the first insights into the diversification of this Cladophorales species flock and contributes to the understanding of speciation in freshwater algae.</p>

Speciation in the Cladophorales species flock of ancient Lake Baikal

<p>Understanding speciation is one of the great challenges in evolutionary biology as many of the processes involved in speciation, as well as the forces leading to morphological and genetic differentiation, are not fully understood. Three main modes of speciation have been described: allopatric, parapatric and sympatric. Sympatric speciation is the most enigmatic mode because in the absence of physical barriers, disruptive selection, assortative mating and hybridization play central roles in reproductive isolation. Although it is accepted that sympatric speciation is possible, only a few examples of this process exist to date. Another common method of speciation in plants and algae is via polyploidization. Recently, a promising system to study speciation in sympatry was discovered: the endemic Cladophorales species flock in ancient Lake Baikal, Russia. The flock consists of sixteen taxa grouped in four genera: Chaetocladiella, Chaetomorpha, Cladophora and Gemmiphora. In spite of their morphological diversity, recent molecular analyses have shown that this is a monophyletic group with low genetic variation and nested within the morphologically simple genus Rhizoclonium. Due to their high number of species, endemism and sympatric distribution, many interesting questions have arisen such as what processes are involved in speciation, and whether this group might be a novel example of sympatric speciation. In this study, we analysed the population genetics of the endemic Baikalian Cladophorales to infer the processes shaping the evolution of the group. First, a set of microsatellites was designed using high-throughput sequencing data. Second, species delimitation methods based on genetic clustering were performed. Third, the population genetics of three widely distributed species was analysed looking for evidence of panmixia, a common criteria to support sympatric speciation. A total of 11 microsatellites that mostly cross-amplify between most species were obtained. The genotyping revealed that most loci had more than two alleles per individual indicating polyploidy. As such, the analyses required a different approach which consisted in coding the genotypes as ‘allelic phenotypes’, allowing the use of individuals of different ploidy levels in the same data set. The species delimitation of 15 operative morphotaxa and 727 individuals supported reproductive isolation of five morphotaxa and two hypotheses of conspecificity. However, some morphotaxa showed unclear assignments revealing the need of further research to clarify their reproductive limits. Finally, the population genetics of Chaetomorpha moniliformis, Cladophora compacta and Cl. kursanovii revealed patterns of genetic variation and structure that suggest different reproductive strategies and dispersal abilities. This demonstrates that contrasting biological characteristics may arise in closely related lineages: Chaetomorpha moniliformis with dominant asexual reproduction and long dispersal abilities; Cladophora compacta with high genetic diversity, no population structure and likely to reproduce sexually; Cl. kursanovii with a structure congruent with geographic distribution and more restricted dispersal. The results suggest that polyploidy, rather than speciation with gene flow, is the force driving the reproductive isolation and evolution of this flock. Although many questions remain to be studied, this research provides the first insights into the diversification of this Cladophorales species flock and contributes to the understanding of speciation in freshwater algae.</p>

Hybphaser identifies hybrid evolution in Australian Thelypterid ferns

Hybridisation can lead to reproductive isolation and consequently speciation. It has been proposed to play an important role in fern evolution, but has been difficult to investigate. This study explores the utility of target sequence capture and reference guided read phasing to investigate the role of evolutionary reticulation in ferns using Australian Thelypteridaceae as a model. The bioinformatics workflow HybPhaser was used to assess divergence between alleles, phase sequence reads to references to construct accessions resembling parental haplotpes, and include them in phylogenetic and network analyses to detect hybrids and parentage. This approach identified two novel hybrid lineages in Thelypteridaceae, one occurring between two different genera (Abacopteris and Christella), and provided evidence that reticulation is likely to have played an important role in the diversification of Australian thelypterids. In addition, hybrid phasing successfully reduced conflicting data and improved overall resolution in the Thelypteridaceae phylogeny, highlighting the power of this approach for reconstructing evolutionary history in reticulated lineages.

Extensive introgression despite Haldane’s rule: insights from grasshopper hybrid zones

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.

Limited movement of a hybrid zone in relation to regional variation in magnitude of climate change

Hybrid zones can provide clear documentation of range shifts in response to climate change and identify loci important to reproductive isolation. Using a deep temporal (36-38 years) comparison of the black-capped (Poecile atricapillus) and Carolina (P. carolinensis) chickadee hybrid zone, we investigated movement of the under-sampled western portion of the zone (western Missouri) as well as investigating whether loci and pathways underpinning reproductive isolation were similar to those from the eastern portion of the hybrid zone. Using 92 birds sampled along the hybrid zone transect in 2016, 68 birds sampled between 1978 and 1980, and 5 additional reference birds sampled from outside the hybrid zone, we generated 11,669 SNPs via ddRADseq. We used these SNPs to interpolate spatially and assess the movement of the hybrid zone interface through time, and to assess variation in introgression among loci. We demonstrate that the interface has moved approximately 5-8 km to the northwest over the last 36-38 years, i.e., at only one-fifth the rate at which the eastern portion of the hybrid zone (e.g. Pennsylvania, Ohio) has moved. Temperature trends across the last 38 years reveal that eastern areas have warmed 50% more than western areas in terms of annual mean temperature, possibly providing an explanation for the slower movement of the hybrid zone in Missouri. Using genomic cline analyses, we detected four genes that showed restricted introgression in both Missouri and Pennsylvania, including Pnoc, a gene involved in metabolism, learning and memory, concordant with previous physiological and behavioral findings on hybrids and the parental species.