The Genealogical Divergence Index Across a Speciation Continuum in Hercules Beetles

The genealogical divergence index (gdi) was developed to aid in molecular species delimitation under the multispecies coalescent model, which has been shown to delimit genetic structures but not necessarily species. Although previous studies have used meta-analyses to show that gdi could be informative for distinguishing taxonomically good species, the biological and evolutionary implications of divergences showing different gdi values have yet to be studied. I showed that an increase in gdi value was correlated with later stages of divergence further along a speciation continuum in an Amazonian Hercules beetle system. Specifically, a gdi value of 0.7 or higher was associated with diverge between biological species that can coexist in geographic proximity while maintaining their evolutionary independence. Divergences between allopatric species that were conventionally given subspecific status, such as geographic taxa that may or may not be morphologically divergent, had gdi values that fell within the species delimitation ambiguous zone (0.2 < gdi < 0.7). However, the results could be drastically affected by the sampling design, i.e., the choice of different geographic populations and the lumping of distinct genetic groups when running the analyses. Different gdi values may prove to be biologically and evolutionarily informative should additional speciation continua from different empirical systems be investigated, and the results obtained may help with objectively delimiting species in the era of integrative taxonomy.

Conserved genomic landscapes of differentiation across Populus speciation continuum

Investigating genome-wide variation patterns along a speciation continuum is of central importance to understand the evolutionary processes contributing to lineage diversification. To identify which forces have shaped the genomic landscapes in Populus, we resequenced 201 whole-genomes from eight closely related species, with pairs of species at different stages along the speciation continuum. Using population structure and identity by descent analyses, we show extensive introgression between some species pairs, especially those with parapatric distributions. Inference of historical changes in effective population sizes support species-specific demographic trajectories, including recent population expansions in species characterized by broad present-day distributions. We observe highly conserved genomic landscapes, either focusing on within-species (genetic diversity: π and recombination rate: ρ) or among-species variation (relative divergence: FST and absolute divergence: DXY). Independent of the stage across the divergence continuum, we recovered positive correlations between the pair π and ρ and the pair DXY and ρ across all species pairs, which is consistent with a substantial contribution of linked selection in shaping these genomic landscapes. However, the positive correlations between π and DXY became weaker as the overall divergence level (da) increased, suggesting that background selection is not the only factor at play. Positive correlations between FST and DXY in all species pairs, regardless of the rate of gene flow, also indicates the high FST could be due to divergent sorting of ancient polymorphism before speciation. Our study showcases the importance of investigating genomic patterns on multiple species across the speciation continuum to better understand the genomic landscapes of diversity and differentiation.

An introgression breakthrough left by an anthropogenic contact between two ascidians

Human-driven translocations of species have diverse evolutionary consequences such as promoting hybridization between previously geographically isolated taxa. This is well-illustrated by the solitary tunicate, Ciona robusta, native to the North East Pacific and introduced in the North East Atlantic. It is now co-occurring with its congener C. intestinalis in the English Channel, and C. roulei in the Mediterranean Sea. Despite their long allopatric divergence, first and second generation crosses showed a high hybridization success between the introduced and native taxa in the laboratory. However, previous genetic studies failed to provide evidence of recent hybridization between C. robusta and C. intestinalis in the wild. Using SNPs obtained from ddRAD-sequencing of 397 individuals from 26 populations, we further explored the genome-wide population structure of the native Ciona taxa. We first confirmed results documented in previous studies, notably i) a chaotic genetic structure at regional scale, and ii) a high genetic similarity between C. roulei and C. intestinalis, which is calling for further taxonomic investigation. More importantly, and unexpectedly, we also observed a genomic hotspot of long introgressed C. robusta tracts into C. intestinalis genomes at several locations of their contact zone. Both the genomic architecture of introgression, restricted to a 1.5 Mb region of chromosome 5, and its absence in allopatric populations suggest introgression is recent and occurred after the introduction of the non-indigenous species. Overall, our study shows that anthropogenic hybridization can be effective in promoting introgression breakthroughs between species at a late stage of the speciation continuum.

Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in ‘the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal (‘asexual’) hybrid vertebrates, where ‘asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of ‘asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5–22% based on mtDNA). These ‘asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid ‘asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, ‘asexuality' and polyploidy. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Parallel evolution of phenological isolation across the speciation continuum in serpentine-adapted annual wildflowers

Understanding the relative importance of reproductive isolating mechanisms across the speciation continuum remains an outstanding challenge in evolutionary biology. Here, we examine a common isolating mechanism, reproductive phenology, between plant sister taxa at different stages of adaptive divergence to gain insight into its relative importance during speciation. We study 17 plant taxa that have independently adapted to inhospitable serpentine soils, and contrast each with a nonserpentine sister taxon to form pairs at either ecotypic or species-level divergence. We use greenhouse-based reciprocal transplants in field soils to quantify how often flowering time (FT) shifts accompany serpentine adaptation, when FT shifts evolve during speciation, and the genetic versus plastic basis of these shifts. We find that genetically based shifts in FT in serpentine-adapted taxa are pervasive regardless of the stage of divergence. Although plasticity increases FT shifts in five of the pairs, the degree of plasticity does not differ when comparing ecotypic versus species-level divergence. FT shifts generally led to significant, but incomplete, reproductive isolation that did not vary in strength by stage of divergence. Our work shows that adaptation to a novel habitat may predictably drive phenological isolation early in the speciation process.

Eunuchs or Females? Causes and Consequences of Gynodioecy on Morphology, Ploidy, and Ecology of Stellaria graminea L. (Caryophyllaceae)

Plant speciation results from intricate processes such as polyploidization, reproductive strategy shifts and adaptation. These evolutionary processes often co-occur, blurring their respective contributions and interactions in the speciation continuum. Here, relying on a large-scale study, we tested whether gynodioecy triggers the divergent evolution of flower morphology and genome between sexes, and contributes to the establishment of polyploids and colonization of ecological niches in Stellaria graminea. We found that gynodioecy in S. graminea leads to flower morphology divergence between females and hermaphrodites, likely due to sexual selection. Contrary to our expectations, gynodioecy occurs evenly in diploids and tetraploids, suggesting that this reproductive strategy was not involved in the establishment of polyploids. Both diploid and tetraploid females have a larger genome size than hermaphrodites, suggesting the presence of sex chromosomes. Finally, ecology differs between cytotypes and to a lesser extent between sexes, suggesting that the link between environment and presence of females is indirect and likely explained by other aspects of the species’ life history. Our study shows that gynodioecy leads to the consistent evolution of sexual traits across a wide range of populations, cytotypes and environments within a given species, and this likely contributes to the phenotypic and genetic distinctiveness of the species from its sister clades.

Isolation and re-connection: the formation of a ring-shaped speciation continuum in an odorous frog (Odorrana margaretae)

The Green Odorous Frog (Odorrana margaretae) around the Sichuan Basin of western China displays a ring-shaped distributional pattern and possesses multiple replicate contact zones between lineages at various levels of differentiation. To understand its unique speciation history and mechanisms, we obtained 1,540 SNPs from 29 populations and 227 individuals using ddRAD sequencing. Population structure analysis revealed three groups within the species: The West, the North & South, and the East groups. These groups were initially isolated at ~2.03 million years ago, and subsequent post-glacial expansion produced the current ring-shaped distribution around Sichuan Basin with three contact zones. Hybridization in those zones involved lineages with different levels of divergence and produced greatly different outcomes. Both the hybrid zones at southwest (S-W) and southeast (E-NS) of the Basin have extensive admixture and less barrier effect. Consequently, the southern region has the highest genetic diversity and becomes an ‘evolutionary melting pot’. In contrast, the hybrid zone at northwestern corner (N-W), which resembles the overlap zone between two expansion terminals of a ring species, has limited admixture with a narrow geographic cline, suggesting partial reproductive isolation between the northern and western populations. The three hybrid zones likely resemble three time points along a speciation continuum; while both E-NS and S-W hybrid zones are merging, the N-W zone may have passed the ‘tipping point’ and is destined for a complete reproductive isolation over time.

Mitochondrial genomics reveals the evolutionary history of the porpoises (Phocoenidae) across the speciation continuum

Historical variation in food resources is expected to be a major driver of cetacean evolution, especially for the smallest species like porpoises. Despite major conservation issues among porpoise species (e.g., vaquita and finless), their evolutionary history remains understudied. Here, we reconstructed their evolutionary history across the speciation continuum. Phylogenetic analyses of 63 mitochondrial genomes suggest that porpoises radiated during the deep environmental changes of the Pliocene. However, all intra-specific subdivisions were shaped during the Quaternary glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent evolution to coastal versus oceanic environments. This suggests that similar mechanisms are driving species diversification in northern (harbor and Dall’s) and southern species (spectacled and Burmeister’s). In contrast to previous studies, spectacled and Burmeister’s porpoises shared a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size since the last 5,000 years. Cryptic lineages within Dall’s, spectacled and Pacific harbor porpoises suggest a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanisms driving diversification in porpoises and an evolutionary framework for their conservation.