Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldane's rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

Diverging patterns of introgression from Schistosoma bovis across S. haematobium African lineages

Hybridization is a fascinating evolutionary phenomenon that raises the question of how species maintain their integrity. Inter-species hybridization occurs between certain Schistosoma species that can cause important public health and veterinary issues. In particular hybrids between Schistosoma haematobium and S. bovis associated with humans and animals respectively are frequently identified in Africa. Recent genomic evidence indicates that some S. haematobium populations show signatures of genomic introgression from S. bovis. Here, we conducted a genomic comparative study and investigated the genomic relationships between S. haematobium, S. bovis and their hybrids using 19 isolates originating from a wide geographical range over Africa, including samples initially classified as S. haematobium (n = 11), S. bovis (n = 6) and S. haematobium x S. bovis hybrids (n = 2). Based on a whole genomic sequencing approach, we developed 56,181 SNPs that allowed a clear differentiation of S. bovis isolates from a genomic cluster including all S. haematobium isolates and a natural S. haematobium-bovis hybrid. All the isolates from the S. haematobium cluster except the isolate from Madagascar harbored signatures of genomic introgression from S. bovis. Isolates from Corsica, Mali and Egypt harbored the S. bovis-like Invadolysin gene, an introgressed tract that has been previously detected in some introgressed S. haematobium populations from Niger. Together our results highlight the fact that introgression from S. bovis is widespread across S. haematobium and that the observed introgression is unidirectional.

Admixture Analysis Using Genotyping-by-Sequencing Reveals Genetic Relatedness and Parental Lineage Distribution in Highbush Blueberry Genotypes and Cross Derivatives

Blueberries (Vaccinium section Cyanococcus) are perennial shrubs widely cultivated for their edible fruits. In this study, we performed admixture and genetic relatedness analysis of northern highbush (NHB, primarily V. corymbosum) and southern highbush (SHB, V. corymbosum introgressed with V. darrowii, V. virgatum, or V. tenellum) blueberry genotypes, and progenies of the BNJ16-5 cross (V. corymbosum × V. darrowii). Using genotyping-by-sequencing (GBS), we generated more than 334 million reads (75 bp). The GBS reads were aligned to the V. corymbosum cv. Draper v1.0 reference genome sequence, and ~2.8 million reads were successfully mapped. From the alignments, we identified 2,244,039 single-nucleotide polymorphisms, which were used for principal component, haplotype, and admixture analysis. Principal component analysis revealed three main groups: (1) NHB cultivars, (2) SHB cultivars, and (3) BNJ16-5 progenies. The overall fixation index (FST) and nucleotide diversity for NHB and SHB cultivars indicated wide genetic differentiation, and haplotype analysis revealed that SHB cultivars are more genetically diverse than NHB cultivars. The admixture analysis identified a mixture of various lineages of parental genomic introgression. This study demonstrated the effectiveness of GBS-derived single-nucleotide polymorphism markers in genetic and admixture analyses to reveal genetic relatedness and to examine parental lineages in blueberry, which may be useful for future breeding plans.

When polymorphism and monomorphism meet: discordant genomic and phenotypic clines across a lizard contact zone

Colour polymorphism can promote rapid evolution and speciation, particularly when populations differ in the number or composition of morphs. The contact zone between Ctenophorus modestus (swift dragon) and C. decresii (tawny dragon) is a compelling study system in which to examine evolutionary processes and outcomes when polymorphic and monomorphic populations meet. Ctenophorus modestus is polymorphic for male throat coloration and lacks ultraviolet (UV) reflectance while C. decresii is monomorphic with UV-blue throats. We characterised genomic and phenotypic clines across the contact zone based on single nucleotide polymorphisms, the mitochondrial ND4 gene, and male colour traits, and concurrently assessed the phenotype of captive-bred F1 hybrids. Our results indicate that genomic introgression is asymmetric, with high frequencies of backcrossing to C. modestus but not C. decresii, accompanied by the prevalence of the C. modestus mtDNA haplotype in hybrids. The clines for throat phenotype are abrupt and displaced towards the range of C. decresii, relative to the genetic and dorsolateral phenotype clines. By contrast, both throat and dorsolateral phenotypes in captive-bred F1 hybrids are intermediate. Our results are consistent with the hypothesis that throat coloration, a polymorphic sexual signal in C. modestus, is the target of selection during incipient speciation and provide insight into the microevolutionary processes that may link polymorphism and speciation.

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

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.

Alternative facts: a reconsideration of putatively natural interspecific hybrid specimens in the genus Heliconius (Lepidoptera: Nymphalidae)

Mallet et al. (2007 BMC Evolutionary Biology, 7, 28) employed a database of putative interspecific hybrid specimens of the genus Heliconius to advance a hypothesis of "the species boundary as a continuum." Here, each of those specimens, as well as subsequently documented specimens, is individually reassessed regarding its phenotype, potential parentage and chain of custody in collections. Using a quantified scale of reliability, most of the specimens are interpreted differently than Mallet et al.'s identifications, and the actual number of interspecific hybrids is estimated to be much smaller than they proposed. To be specific, of 163 putative hybrid specimens examined, 11% suffered from ambiguous identity, 5% from confounding issues with their data labels, 50% were arguably intraspecific (depending upon alternative species concepts), and 22% were almost certainly reared, commercial specimens. Only eleven of the specimens meet the criteria established here to be legitimate and reliable interspecific hybrids, and all of those are between closely-related species. This result has potentially important implications for current hypotheses of frequent genomic introgression of wing pattern alleles among Heliconius clades.

Genomic evidence of globally widespread admixture from polar bears into brown bears during the last ice age

Recent genomic analyses have provided substantial evidence for past periods of gene flow from polar bears (Ursus maritimus) into Alaskan brown bears (Ursus arctos), with some analyses suggesting a link between climate change and genomic introgression. However, because it has only been possible to sample bears from the present day, the timing, frequency, and evolutionary significance of this admixture remains unknown. Here, we analyze genomic DNA from three additional and geographically distinct brown bear populations, including two that lived temporally close to the peak of the last ice age. We find evidence of admixture in all three populations, suggesting that admixture between these species has been common in their recent evolutionary history. In addition, analyses of ten fossil bears from the now-extinct Irish population indicate that admixture peaked during the last ice age, when brown bear and polar bear ranges overlapped. Following this peak, the proportion of polar bear ancestry in Irish brown bears declined rapidly until their extinction. Our results support a model in which ice age climate change created geographically widespread conditions conducive to admixture between polar bears and brown bears, as is again occurring today. We postulate that this model will be informative for many admixing species pairs impacted by climate change. Our results highlight the power of paleogenomes to reveal patterns of evolutionary change that are otherwise masked with only contemporary data.