Temporal variation of effective population size and gene flow determine current patterns of genetic diversity within species, and hence the genetic variation upon which natural selection can act. Although such demographic processes are well understood in terrestrial organisms, they remain largely unknown in the ocean, where species diversity is still being described. Here, we present one of the first population genomic studies in a cephalopod, Octopus insularis, which is distributed in coastal and oceanic island habitats in the Atlantic Ocean, Mexican Gulf and the Caribbean Sea. Using genomic data, we identify the South Equatorial current as the main barrier to gene flow between southern and northern parts of the range, followed by discontinuities in the habitat associated with depth. We find that genetic diversity of insular populations significantly decreases after colonization from the continental shelf, also reflecting low habitat availability. Using demographic modelling, we find signatures of a stronger population expansion for coastal relative to insular populations, consistent with estimated increases in habitat availability since the Last Glacial Maximum. The direction of gene flow is coincident with unidirectional currents and bidirectional eddies between otherwise isolated populations, suggesting that dispersal through pelagic paralarvae is determinant for population connectivity. Together, our results show that oceanic currents and habitat breaks are determinant in the diversification of marine species, shaping standing genetic variability within populations. Moreover, our results show that insular populations are particularly vulnerable to current human exploitation and selective pressures, calling the revision of their protection status.

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.

In 1859, Charles Darwin proposed that species are not fundamentally different from subspecies or the varieties from which they evolve. A century later, Dobzhansky (1958) suggested that many such lineages are ephemeral and are likely to revert differentiation through introgression (Fig. 1A); only a few evolve complete reproductive isolation and persist in sympatry. In this issue of Molecular Ecology, Bouzid et al. (2021) show how new analytical methods, when applied to genome data, allow us to more precisely determine whether or not species formation follows the paths outlined by Darwin and Dobzhansky (Fig. 1B). The authors study the diversification of the lizard Sceloporus occidentalis, finding a continuum of genetic interactions between the preservation of genetic identity to genetic merger, analogous to what is exemplified by ring species. In doing so, they teach us two tales on species formation: that lineages are fractal byproducts of evolutionary processes such as genetic drift and selection, and that lineages are often ephemeral and do not always progress into species. Studying ephemeral lineages like those in S. occidentalis allows us to capture divergence at its earliest stages, and potentially to determine the factors that allow lineages to remain distinct despite pervasive gene flow. These lineages thus serve as a natural laboratory to address long standing hypotheses on species formation.

Vector-borne pathogens exist in obligate transmission cycles between vector and reservoir host species. Host shifts can lead to geographic expansion and the emergence of new diseases. Three etiological agents of human Lyme borreliosis (Borrelia afzelii, Borrelia bavariensis, and Borrelia garinii) predominantly utilize two distinct tick species as vectors in Asia (Ixodes persulcatus) and Europe (Ixodes ricinus) but how and in which order they colonized each continent remains unknown. Here, by reconstructing the evolutionary history of 142 Eurasian isolates, we show that all three Borrelia genospecies evolved from an Asian origin, suggesting that successful expansion into Europe resulted through invading a novel vector. The pattern of gene flow between continents is different between genospecies and most likely conditioned by reservoir host association and their dispersal. Our results highlight that Eurasian Lyme borreliosis agents are all capable of geographic expansion through vector shifts, but potentially differ in their capacity as emergent pathogens.

Reproductive isolation is often achieved when genes that are neutral or beneficial in their genomic background become functionally incompatible in a foreign genome, causing inviability, sterility or low fitness in hybrids. Recent studies suggest that mitonuclear interactions are among the initial incompatibilities to evolve at early stages of population divergence across taxa. Yet, it is unclear whether mitonuclear incompatibilities involve few or many regions in the nuclear genome. We employ an experimental evolution approach starting with unfit F2 interpopulation hybrids of the copepod Tigriopus californicus, in which compatible and incompatible nuclear alleles compete in a fixed mitochondrial background. After about nine generations, we observe a generalized increase in population size and in survivorship, suggesting efficiency of selection against maladaptive phenotypes. Whole genome sequencing of evolved populations showed some consistent allele frequency changes across the three replicates of each reciprocal cross, but markedly different patterns between mitochondrial background. In only a few regions (~6.5% of the genome), the same parental allele was overrepresented irrespective of the mitochondrial background. About 33% of the genome shows allele frequency changes consistent with divergent selection, with the location of these genomic regions strongly differing between mitochondrial backgrounds. The dominant allele matches the mitochondrial background in 87 and 89% of these genomic regions, consistent with mitonuclear coadaptation. These results suggest that mitonuclear incompatibilities have a complex polygenic architecture that differs between populations, potentially generating genome wide barriers to gene flow between closely related taxa.

Theoretical and empirical studies have shown that species radiations are facilitated when a trait under divergent natural selection is also involved in sexual selection. It is yet unclear how quick and effective radiations are where sexual selection is unrelated to the ecological environment. We address this question using grasshopper species of the genus Chorthippus, which have evolved strong assortative mating while lacking noticeable eco-morphological divergence. Mitochondrial genomes suggest that the radiation is relatively recent, dating to the mid-Pleistocene, which leads to extensive incomplete lineage sorting throughout the mitochondrial and the nuclear genomes. Nuclear data show extremely low genomic differentiation among species, yet hybrids are absent in sympatric localities. Demographic analyses shed some light into these seemingly contradictory patterns. The estimated demographic model shows a long period of geographic isolation, followed by secondary contact and extensive introgression. This suggests that an initial period of geographic isolation might favor the coupling of male signaling and female preference, which currently maintains species boundaries in the face of long-term gene flow. More generally, these results suggest that sexual selection can lead to radiations without a primary role of divergent natural selection, resulting in cryptic species that are genetically, morphologically and ecologically similar, but otherwise behave mostly as good biological species.

Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, particularly regarding highly vulnerable marine ecosystems. Although a large effort has been made to design Marine Protected Areas (MPAs) worldwide, it is still unclear how many species actually exist in these MPAs, what is the genetic connectivity between areas with different protective regimes, and what is their relative genetic diversity. We answer these questions using morphologically cryptic species of the genus Mugil that are sympatric in the largest MPA in the Tropical Southwestern marine province. Population structure analyses show the existence of five highly divergent species (FST > 0.855) and no genetic divergence between two estuaries with different protection status (FST = 0.005). Sympatric individuals are assigned to single clusters and show strong concordance among hundreds of independent gene trees, consistent with full reproductive isolation and no ancestral nor ongoing hybridization. Differences of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions during the evolutionary history of these species, rather than recent impact of fisheries. Together, our results suggest that designing MPAs with areas of integral protection in between areas where fisheries are permitted could be an effective way to manage cryptic species that cannot have species-specific quotas. More generally, this work shows a cost-efficient approach that is transferable to other marine or terrestrial organisms of special concern, helping to implement science-based regulations for management and conservation.