Geographic Variation in Genomic Signals of Admixture Between Two Closely Related European Sepsid Fly Species.

UNLABELLED The extent of interspecific gene flow and its consequences for the initiation, maintenance, and breakdown of species barriers in natural systems remain poorly understood. Interspecific gene flow by hybridization may weaken adaptive divergence, but can be overcome by selection against hybrids, which may ultimately promote reinforcement. An informative step towards understanding the role of gene flow during speciation is to describe patterns of past gene flow among extant species. We investigate signals of admixture between allopatric and sympatric populations of the two closely related European dung fly species Sepsis cynipsea and S. neocynipsea (Diptera: Sepsidae). Based on microsatellite genotypes, we first inferred a baseline demographic history using Approximate Bayesian Computation. We then used genomic data from pooled DNA of natural and laboratory populations to test for past interspecific gene flow based on allelic configurations discordant with the inferred population tree (ABBA-BABA test with D-statistic). Comparing the detected signals of gene flow with the contemporary geographic relationship among interspecific pairs of populations (sympatric vs. allopatric), we made two contrasting observations. At one site in the French Cevennes, we detected an excess of past interspecific gene flow, while at two sites in Switzerland we observed lower signals of past microsatellite genotypes gene flow among populations in sympatry compared to allopatric populations. These results suggest that the species boundaries between these two species depend on the past and/or present eco-geographic context in Europe, which indicates that there is no uniform link between contemporary geographic proximity and past interspecific gene flow in natural populations. SUPPLEMENTARY INFORMATION The online version contains supplementary material available at 10.1007/s11692-023-09612-5

Geographic Variation in Genomic Signals of Admixture Between Two Closely Related European Sepsid Fly Species

The extent of interspecific gene flow and its consequences for the initiation, maintenance, and breakdown of species barriers in natural systems remain poorly understood. Interspecific gene flow by hybridization may weaken adaptive divergence, but can be overcome by selection against hybrids, which may ultimately promote reinforcement. An informative step towards understanding the role of gene flow during speciation is to describe patterns of past gene flow among extant species. We investigate signals of admixture between allopatric and sympatric populations of the two closely related European dung fly species Sepsis cynipsea and S. neocynipsea (Diptera: Sepsidae). Based on microsatellite genotypes, we first inferred a baseline demographic history using Approximate Bayesian Computation. We then used genomic data from pooled DNA of natural and laboratory populations to test for past interspecific gene flow based on allelic configurations discordant with the inferred population tree (ABBA–BABA test with D-statistic). Comparing the detected signals of gene flow with the contemporary geographic relationship among interspecific pairs of populations (sympatric vs. allopatric), we made two contrasting observations. At one site in the French Cevennes, we detected an excess of past interspecific gene flow, while at two sites in Switzerland we observed lower signals of past microsatellite genotypes gene flow among populations in sympatry compared to allopatric populations. These results suggest that the species boundaries between these two species depend on the past and/or present eco-geographic context in Europe, which indicates that there is no uniform link between contemporary geographic proximity and past interspecific gene flow in natural populations

Geographic patterns of postzygotic isolation between two closely related widespread dung fly species (Sepsis cynipsea and Sepsis neocynipsea; Diptera: Sepsidae)

Identifying the contribution of pre‐ and postzygotic barriers to gene flow is a key goal of speciation research. The widespread dung fly species Sepsis cynipsea and Sepsis neocynipsea offer great potential for studying the speciation process over a range of opportunities for gene exchange within and across sister species (cross‐continental allopatry, continental parapatry and sympatry). We examined the role of postcopulatory isolating barriers by comparing female fecundity and egg‐to‐adult viability of F1 and F2 hybrids, as well as backcrosses of F1 hybrids with the parental species, via replicated crosses of sym‐, para‐ and allopatric populations. Egg‐to‐adult viability was strongly but not totally suppressed in hybrids, and offspring production approached nil in the F2 generation (hybrid breakdown), indicating yet unspecified intrinsic incompatibilities. Viable F1 hybrid offspring showed almost absolute male (the heterogametic sex) sterility while females remained largely fertile, in accordance with Haldane's rule. Hybridization between the two species in European areas of sympatry (Swiss Alps) indicated only minor reinforcement based on fecundity traits. Crossing geographically isolated European and North American S. neocynipsea showed similar albeit weaker isolating barriers that are most easily explained by random genetic drift. We conclude that in this system with a biogeographic continuum of reproductive barriers, speciation is mediated primarily by genetic drift following dispersal of flies over a wide (allopatric) geographic range, with some role of natural or sexual selection in incidental or direct reinforcement of incompatibility mechanisms in areas of European sympatry. S(ubs)pecies status of continental S. neocynipsea appears warranted

Exaggerated male forelegs are not more differentiated than wing morphology in two widespread sister species of black scavenger flies

Sexual selection represents a potent force that can drive rapid population differentiation in traits related to reproductive success. Hence, sexual traits are expected to show greater population divergence than non‐sexual traits. We test this prediction by exploring patterns of morphological differentiation of the exaggerated fore femur (a male‐specific sexual trait) and the wing (a non‐sexual trait) among allopatric and sympatric populations of the widespread sister dung fly species Sepsis neocynipsea and Sepsis cynipsea (Diptera: Sepsidae). While both species occur in Eurasia, S. neocynipsea also abounds in North America, albeit previous studies suggest strong differentiation in morphology, behavior, and mating systems. To evaluate the degree of differentiation expected under neutrality between S. cynipsea, European S. neocynipsea, and North American S. neocynipsea, we genotyped 30 populations at nine microsatellite markers, revealing almost equal differentiation between and minor differentiation among geographic populations within the three lineages. Landmark‐based analysis of 18 populations reared at constant 18 and 24°C in a laboratory common garden revealed moderate temperature‐dependent phenotypic plasticity and significant heritable differentiation in size and shape of male forelegs and wings among iso‐female lines of the three lineages. Following the biological species concept, there was weaker differentiation between cross‐continental populations of S. neocynipsea relative to S. cynipsea, and more fore femur differentiation between the two species in sympatry versus allopatry (presumably due to character displacement). Contrary to expectation, wing morphology showed as much shape differentiation between evolutionary independent lineages as fore femora, providing no evidence for faster diversification of traits primarily engaged in mating

Temporal niche partitioning of Swiss black scavenger flies in relation to season and substrate age (Diptera, Sepsidae)

Understanding why and how multiple species manage to coexist represents a primary goal of ecological and evolutionary research. This is of particular relevance for communities that depend on resource rich ephemeral habitats that are prone to high intra- and interspecific competition. Black scavenger flies (Diptera: Sepsidae) are common and abundant acalyptrate flies associated with livestock dung decomposition in human-influenced agricultural grasslands worldwide. Several widespread sepsid species with apparently very similar ecological niches coexist in Europe, but despite their ecological role and their use in evolutionary ecological research, our understanding of their ecological niches and spatio-temporal distribution is still rudimentary. To gain a better understanding of their ecology, we here investigate niche partitioning at two temporal scales. First, we monitored the seasonal occurrence, often related to thermal preference, over multiple years and sites in Switzerland that differ in altitude. Secondly, we also investigate fine-scale temporal succession on dairy cow pastures. In accordance with their altitudinal and latitudinal distribution in Europe, some species were common over the entire season with a peak in summer, hence classified as warm-loving, whereas others were primarily present in spring or autumn. Phenological differences thus likely contribute to species coexistence throughout the season. However, the community also showed pronounced species turnover related to cow pat age. Some species colonize particularly fresh dung and are gradually replaced by others. Furthermore, the correlation between co-occurrence and phylogenetic distance of species revealed significant under-dispersion, indicating that more closely related species are frequently recovered at the same location. As a whole, our data suggests temporal niche differentiation of closely related species that likely facilitates the rather high species diversity on Swiss cattle pastures. The underlying mechanisms allowing close relatives to co-occur however require further scrutiny

Temporal niche partitioning of Swiss black scavenger flies in relation to season and substrate age (Diptera, Sepsidae)

Understanding why and how multiple species manage to coexist represents a primary goal of ecological and evolutionary research. This is of particular relevance for communities that depend on resource rich ephemeral habitats that are prone to high intra- and interspecific competition. Black scavenger flies (Diptera: Sepsidae) are common and abundant acalyptrate flies associated with livestock dung decomposition in human-influenced agricultural grasslands worldwide. Several widespread sepsid species with apparently very similar ecological niches coexist in Europe, but despite their ecological role and their use in evolutionary ecological research, our understanding of their ecological niches and spatio-temporal distribution is still rudimentary. To gain a better understanding of their ecology, we here investigate niche partitioning at two temporal scales. First, we monitored the seasonal occurrence, often related to thermal preference, over multiple years and sites in Switzerland that differ in altitude. Secondly, we also investigate fine-scale temporal succession on dairy cow pastures. In accordance with their altitudinal and latitudinal distribution in Europe, some species were common over the entire season with a peak in summer, hence classified as warm-loving, whereas others were primarily present in spring or autumn. Phenological differences thus likely contribute to species coexistence throughout the season. However, the community also showed pronounced species turnover related to cow pat age. Some species colonize particularly fresh dung and are gradually replaced by others. Furthermore, the correlation between co-occurrence and phylogenetic distance of species revealed significant under-dispersion, indicating that more closely related species are frequently recovered at the same location. As a whole, our data suggests temporal niche differentiation of closely related species that likely facilitates the rather high species diversity on Swiss cattle pastures. The underlying mechanisms allowing close relatives to co-occur however require further scrutiny