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 may 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 hybridization. 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 add to the few studies on species with X0 sex determination system and contradict the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

Next-generation sequencing, isolation and characterization of 14 microsatellite loci of Canthon cyanellus (Coleoptera: Scarabaeidae).

BACKGROUND: We used Illumina paired-end sequencing to isolate and characterize microsatellites of Canthon cyanellus, a Neotropical roller dung beetle, encompassing several lineages within its distribution range. METHODS AND RESULTS: We examined C. cyanellus specimens collected at eight different localities in Mexico (two or three specimens per locality). We initially performed amplification tests with 16 loci, but two of which were unsuccessful. The 14 remaining microsatellites were polymorphic, with 2-16 alleles each. The expected and observed heterozygosity ranged from 0.11 to 0.76 and from 0.20 to 0.78, respectively. CONCLUSIONS: These microsatellites will help to assess structure at the population and lineage levels, identify zones of potential hybridization between lineages, and draw a more precise geographic delimitation of C. cyanellus lineages.

The impact of chromosomal fusions on 3D genome folding and recombination in the germ line.

The spatial folding of chromosomes inside the nucleus has regulatory effects on gene expression, yet the impact of genome reshuffling on this organization remains unclear. Here, we take advantage of chromosome conformation capture in combination with single-nucleotide polymorphism (SNP) genotyping and analysis of crossover events to study how the higher-order chromatin organization and recombination landscapes are affected by chromosomal fusions in the mammalian germ line. We demonstrate that chromosomal fusions alter the nuclear architecture during meiosis, including an increased rate of heterologous interactions in primary spermatocytes, and alterations in both chromosome synapsis and axis length. These disturbances in topology were associated with changes in genomic landscapes of recombination, resulting in detectable genomic footprints. Overall, we show that chromosomal fusions impact the dynamic genome topology of germ cells in two ways: (i) altering chromosomal nuclear occupancy and synapsis, and (ii) reshaping landscapes of recombination.

Alternative reproductive strategies in black-winged territorial males of Paraphlebia zoe (Odonata, Thaumatoneuridae).

Alternative reproductive strategies are commonly associated with male dimorphism. In Paraphlebia zoe, a species of damselfly whose males are dimorphic in wing coloration, black-and-white-winged (BW) males defend territories, while hyaline-winged (HW) males usually play the role of satellites. We found that several BW males can sometimes share a territory, and we hypothesized that within this morph there are two alternative tactics: submissive and dominant. We conducted an experiment to test whether dominant and submissive roles are plastic or stable and fixed on each individual. To this end, we manipulated black and white spots of BW males in four treatments: (i) painting over white and black spots without changing their size, (ii) erasing the white spot using black painting, (iii) increasing the black spot and moving the white spot maintaining its size and (iv) control males. Additionally, we investigated the correlation between some phenotypic variables (wing asymmetry, survival and recapture probabilities) and male behaviour (in terms of quality of the territory). We found that the two behavioural roles (submissive and dominant) were not affected by the manipulative experiments, therefore suggesting that they are stable and fixed. Additionally, we found a positive correlation between body size and survival in both sexes, and a positive effect of territory quality and lifespan on mating success. Moreover, the largest and youngest BW males were the most symmetrical. We conclude that Paraphlebia zoe holds high behavioural diversity, with two types of strategies in BW males, dominant and submissive. The occurrence of this intra-morph behavioural diversity might depend on demographic factors such as population density and/or the relative frequency of the different morphs.

Nonadaptive radiation in damselflies.

Adaptive radiations have long served as living libraries to study the build-up of species richness; however, they do not provide good models for radiations that exhibit negligible adaptive disparity. Here, we review work on damselflies to argue that nonadaptive mechanisms were predominant in the radiation of this group and have driven species divergence through sexual selection arising from male-female mating interactions. Three damselfly genera (Calopteryx,Enallagma and Ischnura) are highlighted and the extent of (i) adaptive ecological divergence in niche use and (ii) nonadaptive differentiation in characters associated with reproduction (e.g. sexual morphology and behaviours) was evaluated. We demonstrate that species diversification in the genus Calopteryx is caused by nonadaptive divergence in coloration and behaviour affecting premating isolation, and structural differentiation in reproductive morphology affecting postmating isolation. Similarly, the vast majority of diversification events in the sister genera Enallagma and Ischnura are entirely driven by differentiation in genital structures used in species recognition. The finding that closely related species can show negligible ecological differences yet are completely reproductively isolated suggests that the evolution of reproductive isolation can be uncoupled from niche-based divergent natural selection, challenging traditional niche models of species coexistence.

Mammalian Comparative Genomics Reveals Genetic and Epigenetic Features Associated with Genome Reshuffling in Rodentia.

Understanding how mammalian genomes have been reshuffled through structural changes is fundamental to the dynamics of its composition, evolutionary relationships between species and, in the long run, speciation. In this work, we reveal the evolutionary genomic landscape in Rodentia, the most diverse and speciose mammalian order, by whole-genome comparisons of six rodent species and six representative outgroup mammalian species. The reconstruction of the evolutionary breakpoint regions across rodent phylogeny shows an increased rate of genome reshuffling that is approximately two orders of magnitude greater than in other mammalian species here considered. We identified novel lineage and clade-specific breakpoint regions within Rodentia and analyzed their gene content, recombination rates and their relationship with constitutive lamina genomic associated domains, DNase I hypersensitivity sites and chromatin modifications. We detected an accumulation of protein-coding genes in evolutionary breakpoint regions, especially genes implicated in reproduction and pheromone detection and mating. Moreover, we found an association of the evolutionary breakpoint regions with active chromatin state landscapes, most probably related to gene enrichment. Our results have two important implications for understanding the mechanisms that govern and constrain mammalian genome evolution. The first is that the presence of genes related to species-specific phenotypes in evolutionary breakpoint regions reinforces the adaptive value of genome reshuffling. Second, that chromatin conformation, an aspect that has been often overlooked in comparative genomic studies, might play a role in modeling the genomic distribution of evolutionary breakpoints.

Climate-induced range shifts and possible hybridisation consequences in insects.

Many ectotherms have altered their geographic ranges in response to rising global temperatures. Current range shifts will likely increase the sympatry and hybridisation between recently diverged species. Here we predict future sympatric distributions and risk of hybridisation in seven Mediterranean ischnurid damselfly species (I. elegans, I. fountaineae, I. genei, I. graellsii, I. pumilio, I. saharensis and I. senegalensis). We used a maximum entropy modelling technique to predict future potential distribution under four different Global Circulation Models and a realistic emissions scenario of climate change. We carried out a comprehensive data compilation of reproductive isolation (habitat, temporal, sexual, mechanical and gametic) between the seven studied species. Combining the potential distribution and data of reproductive isolation at different instances (habitat, temporal, sexual, mechanical and gametic), we infer the risk of hybridisation in these insects. Our findings showed that all but I. graellsii will decrease in distributional extent and all species except I. senegalensis are predicted to have northern range shifts. Models of potential distribution predicted an increase of the likely overlapping ranges for 12 species combinations, out of a total of 42 combinations, 10 of which currently overlap. Moreover, the lack of complete reproductive isolation and the patterns of hybridisation detected between closely related ischnurids, could lead to local extinctions of native species if the hybrids or the introgressed colonising species become more successful.

Ontogenetic shifts in male mating preference and morph-specific polyandry in a female colour polymorphic insect.

BACKGROUND: Sexual conflict over mating rates may favour the origin and maintenance of phenotypes with contrasting reproductive strategies. The damselfly Ischnura elegans is characterised by a female colour polymorphism that consists of one androchrome and two gynochrome female morphs. Previous studies have shown that the polymorphism is genetic and to a high extent maintained by negative frequency-dependent mating success that varies temporally and spatially. However, the role of learning in male mating preferences has received little attention. We used molecular markers to investigate differences in polyandry between female morphs. In addition, we experimentally investigated innate male mating preferences and experience-dependent shifts in male mating preferences for female morphs. RESULTS: Field and molecular data show that androchrome females were less polyandrous than gynochrome females. Interestingly, we found that naïve males showed significantly higher sexual preferences to androchrome than to gynochrome females in experimental trials. In contrast, experienced males showed no preference for androchrome females. CONCLUSIONS: The ontogenetic change in male mate preferences occurs most likely because of learned mate recognition after experience with females, which in this case does not result in a preference for one of the morphs, but rather in the loss of an innate preference for androchrome females.