Fifth mass extinction event triggered the diversification of the largest family of freshwater gastropods (Caenogastropoda: Truncatelloidea: Hydrobiidae).

The fifth mass extinction event (MEE) at the Cretaceous-Palaeogene (K-Pg) boundary 66 million years ago (Ma) led to massive species loss but also triggered the diversification of higher taxa. Five models have been proposed depending on whether this diversification occurred before, during or after the K-Pg boundary and the rate of species accumulation. While the effects of the K-Pg MEE on vertebrate evolution are relatively well understood, the impact on invertebrates, particularly in freshwater ecosystems, remains controversial. One example is the hyperdiverse Hydrobiidae-the most species-rich family of freshwater gastropods. Whereas some studies place its origin in the Jurassic or even Carboniferous, most fossil records postdate the K-Pg event. We therefore used robustly time-calibrated multi-locus phylogenies of >400 species representing >100 hydrobiid genera to unravel its evolutionary history and patterns of diversification. We found that the family started diversifying shortly after the K-Pg boundary (∼60 Ma; 95% highest posterior density 52-69 Ma). Lineage richness gradually increased to the present and phylogenetic diversity until ∼25 Ma. These findings suggest that diversification was not initially driven by ecological opportunity. Combining the two criteria of timing and rate of diversification, a soft-explosive diversification model of aquatic vertebrates best fits the patterns observed. We also show that most higher hydrobiid taxa (i.e. subfamilies) diversified from the Middle Oligocene to Middle Miocene (i.e. 12-28 Ma). Two of the 15 major clades delimited are described here as new subfamilies (i.e. Bullaregiinae n. subfam. and Pontobelgrandiellinae n. subfam.), whose members are restricted to subterranean waters. Our results are an important contribution to understanding how the fifth MEE has shaped evolution and patterns of biodiversity in continental aquatic systems. Given the high extinction risks faced by many hydrobiids today, they also emphasise the need to study the biodiversity of vulnerable ecosystems.

Recurrent founder-event speciation across the Mediterranean likely shaped the species diversity and geographic distribution of the freshwater snail genus Mercuria Boeters, 1971 (Caenogastropoda: Hydrobiidae).

Dispersal is known to play an important role in shaping the diversity and geographic range of freshwater gastropods. Here, we used phylogenetic methods to test for the influence of dispersal and other biogeographic processes (such as vicariance) on the speciation and distribution patterns of Mercuria Boeters, 1971, a snail genus widely distributed in the western Palaearctic. The 25 extant species traditionally thought to comprise the genus, which were described mainly on the basis of morphology, have been recorded from lowland waters in both the Mediterranean and Atlantic river basins of Europe and North Africa. Using molecular phylogenies based on three gene fragments (COI, 16S rRNA and 28S rRNA) from 209 individuals, four molecular species delimitation methods and a shell characterization, we identified 14 putative species in our dataset, nine of which correspond to species classified by traditional taxonomy. Furthermore, biogeographical modelling favoured a scenario in which recurrent founder-event speciation since the late Miocene is the most probable process explaining the species diversity and distribution of the Mediterranean clades, whereas episodes of postglacial northward colonization from Iberian refugia by the species M.tachoensis may explain the current presence of the genus in Atlantic lowlands. The dispersal events inferred for Mercuria, probably promoted by multiple factors such as the changing connectivity of drainage basins driven by climate change or better access for avian dispersal vectors in lowlands, may explain the rare case among hydrobiids of a species-rich genus containing individual species with a large distribution area.

Drivers of diversification in freshwater gastropods vary over deep time.

Unravelling the drivers of species diversification through geological time is of crucial importance for our understanding of long-term evolutionary processes. Numerous studies have proposed different sets of biotic and abiotic controls of speciation and extinction rates, but typically they were inferred for a single, long geological time frame. However, whether the impact of biotic and abiotic controls on diversification changes over time is poorly understood. Here, we use a large fossil dataset, a multivariate birth-death model and a comprehensive set of biotic and abiotic predictors, including a new index to quantify tectonic complexity, to estimate the drivers of diversification for European freshwater gastropods over the past 100 Myr. The effects of these factors on origination and extinction are estimated across the entire time frame as well as within sequential time windows of 20 Myr each. Our results find support for temporal heterogeneity in the factors associated with changes in diversification rates. While the factors impacting speciation and extinction rates vary considerably over time, diversity-dependence and topography are consistently important. Our study highlights that a high level of heterogeneity in diversification rates is best captured by incorporating time-varying effects of biotic and abiotic factors.

Historical faunal exchange between the Pontocaspian Basin and North America.

Ecrobia is a genus of small brackish-water mud snails with an amphi-Atlantic distribution. Interestingly, the species occurring in the northwestern Atlantic, Ecrobia truncata, is more closely related to the Pontocaspian taxa, Ecrobia grimmi and Ecrobia maritima, than to the species occurring in the northeastern Atlantic and Mediterranean Sea. At least three colonization scenarios may account for this peculiar biogeographical pattern: (1) a recent human-mediated dispersal, (2) a historical transatlantic interchange, and (3) a historical transpolar interchange. To test these three scenarios, we used five operational criteria-time of species divergence, first appearance in the fossil record, dispersal limitation as well as environmental filtering and biotic interactions along the potential migration routes. Specifically, we inferred a time-calibrated molecular phylogeny for Ecrobia and reconstructed a paleogeographical map of the Arctic Ocean at 2.5 million years ago (Mya). Based on the five operational criteria, scenarios 1 and 2 can likely be rejected. In contrast, all criteria support scenario 3 (historical transpolar interchange). It is therefore suggested that a bird-mediated and/or ocean current-mediated faunal interchange via the Arctic Ocean occurred during the Late Pliocene or Early Pleistocene. This dispersal was likely facilitated by reduced distances between the Eurasian and North American/Greenland landmasses, marine introgressions, and/or a stepping-stone system of brackish-water habitats in northern Siberia, as well as a lack of competition along the migration route. As for the direction of dispersal, the scientific data presented are not conclusive. However, there is clearly more support for the scenario of dispersal from the Pontocaspian Basin to North America than vice versa. This is the first study providing evidence for a natural faunal exchange between the Pontocaspian Basin and North America via the Arctic Ocean.

The genus Mercuria Boeters, 1971 in Morocco: first molecular phylogeny of the genus and description of two new species (Caenogastropoda, Truncatelloidea, Hydrobiidae).

The western Palearctic freshwater snail genus Mercuria (Caenogastropoda: Hydrobiidae) comprises 26 species primarily distributed in lowland localities of Western Europe and North Africa. Although this genus in North Africa has received considerable attention in terms of species discoveries through morphological descriptions, its distribution and phylogenetic patterns remain unknown. Based on morphological and mitochondrial DNA (mtCOI) evidence, this study examines the three Mercuria species (M.bakeri, M.tingitana, and M.targouasensis) from Morocco identified so far. Besides expanding on information regarding the anatomy of these species, two new species (M.midarensis sp. n. and M.tensiftensis sp. n.) are described for this region and phylogenetic relationships inferred between these species and the European M.emiliana and M.similis. All Moroccan and European species were recovered as independent entities according to these phylogenetic inferences (uncorrected p-distances 2.8-8.5%) and DNA barcode data. Moroccan Mercuria species clustered with M.emiliana from Spain, although basal relationships within this clade were not well supported. Given that factors such as the season when specimens are collected, habitat type, and parasites could be responsible for the remarkable intraspecific variation observed in shell and penis morphology, it is proposed that the most efficient approach to delimit and identify Mercuria species is to combine morphological descriptions with genetic data.

Ecological opportunity may facilitate diversification in Palearctic freshwater organisms: a case study on hydrobiid gastropods.

BACKGROUND: Differences in species richness among phylogenetic clades are attributed to clade age and/or variation in diversification rates. Access to ecological opportunity may trigger a temporary increase in diversification rates and ecomorphological variation. In addition, lower body temperatures in poikilothermic animals may result in decreasing speciation rates as proposed by the metabolic theory of ecology. For strictly freshwater organisms, environmental gradients within a river continuum, linked to elevation and temperature, might promote access to ecological opportunity and alter metabolic rates, eventually influencing speciation and extinction processes. To test these hypotheses, we investigated the influence of environmental temperature and elevation, as proxies for body temperature and ecological opportunity, respectively, on speciation rates and ecomorphological divergence. As model systems served two closely related gastropod genera with unequal species richness and habitat preferences - Pseudamnicola and Corrosella. RESULTS: Lineage-through-time plots and Bayesian macroevolutionary modeling evidenced that Pseudamnicola species, which typically live in lower reaches of rivers, displayed significantly elevated speciation rates in comparison to the 'headwater genus' Corrosella. Moreover, state-dependent speciation models suggested that the speciation rate increased with decreasing elevation, supporting the ecological opportunity hypothesis. In contrast, a significant effect of environmental temperature, as proposed by the metabolic theory of ecology, could not be observed. Disparity-through-time plots, models of ecomorphological evolution, and ancestral habitat estimation showed for Pseudamnicola species rapid morphological divergence shortly after periods of elevational and habitat divergence. In contrast, Corrosella species did not deviate from null models of drift-like evolution. CONCLUSION: Our finding that speciation rates are correlated with elevation and ecomorphological disparity but not with environmental temperatures suggests that differences in ecological opportunity may have played a key role in Corrosella and Pseudamnicola diversifications. We propose that Pseudamnicola lineages experienced higher ecological opportunity through dispersal to new locations or habitats in lowlands, which may explain the increase in speciation rates and morphological change. In contrast, the evolution of Corrosella in headwaters is likely less facilitated by the environment and more by non-ecological processes.

Living on the mountains: patterns and causes of diversification in the springsnail subgenus Pseudamnicola (Corrosella) (Mollusca: Caenogastropoda: Hydrobiidae).

Hydrobiidae is one of the largest families of freshwater gastropods comprised of approximately 400 genera and 1000 species. Despite this high level of diversity, most hydrobiid species inhabit fragile ecosystems in restricted distribution areas. In this work, we analyze modes of speciation and causes of diversification in the hydrobiid springsnail subgenus Pseudamnicola (Corrosella). Species of this group typically live in nutrient poor springs and streams and are restricted to mountainous regions of the Iberian Peninsula (Spain) and Southern France. Previous morphological and molecular (based only on the cytochrome c oxidase subunit I (COI) gene) studies revealed 11 nominal Corrosella species. In this study, we enhance published molecular results by generating new data from mitochondrial (16S rRNA and COI) and nuclear ribosomal regions (18S and 28S rRNA) from 50 Corrosella populations. As a result of this study we have identified one new species, making a total of twelve recognized species in the subgenus Corrosella. Our phylogenetic results also reveal the existence of three lineages within the subgenus, and the estimation of time divergence indicates the occurrence of three main speciation events during the upper Miocene to Pleistocene. We test the influence of several geographical and ecological variables and observe that diversification patterns are related to habitat fragmentation rather than environmental conditions. This result suggests that the high level of diversity observed within the subgenus may have resulted from a non-adaptive radiation. The formation of the Iberian Peninsula mountain ranges (the Pyrenees in the north and the Betic Cordillera in the south) and the configuration of the Iberian current hydrographic system played important roles in Corrosella speciation. Additionally, during the Miocene the Iberian Peninsula experienced a gradient of increasing temperature and dryness from north to south, which together with a high level of tectonic activity, may have caused the majority of the diversity found in the southern Iberian Peninsula.

Morphological and molecular evidence for cryptic species of springsnails [genus Pseudamnicola ( Corrosella) (Mollusca, Caenogastropoda, Hydrobiidae)].

Several Pseudamnicola (Corrosella) populations of the central and eastern Iberian Peninsula have been ascribed to Pseudamnicola (Corrosella) astieri (Dupuy, 1851), though recent evidence demonstrates the species could be endemic to the departments of Var and Alpes-Maritimes in France. Through the identification of cryptic species using a combined morphological and phylogenetic approach, this paper provides a detailed morphological description of Pseudamnicola (Corrosella) astieri, clarifying its taxonomic boundaries and confirming it as a French endemic. In parallel, by comparing Pseudamnicola (Corrosella) populations from the provinces of Castellón and Valencia in Eastern Spain, it was observed that rather than Pseudamnicola (Corrosella) astieri they represented a new species here described as Pseudamnicola (Corrosella) hauffeisp. n. Among other characters, the two species show marked differences in shell shape, male and female genital systems, radular formula and concentration of the nervous system. Pseudamnicola (Corrosella) hauffeisp. n. was also compared morphologically to another two Pseudamnicola (Corrosella) species living in nearby areas [Pseudamnicola (Corrosella) hinzi Boeters, 1986 and Pseudamnicola (Corrosella) navasiana (Fagot, 1907)], molecularly to Pseudamnicola (Corrosella) falkneri (Boeters, 1970), the type species of the subgenus, and to the rest of the Pseudamnicola (Corrosella) species described so far. Morphological differentiation between the species is supported by a genetic divergence of 7.4% inferred from a partial sequence (658 bp) of the mitochondrial gene cytochrome c oxidase subunit I (COI). On the basis of an average 8% (5.39 to 11.15%) divergence estimated for the COI gene in other Pseudamnicola (Corrosella) species reported in GenBank, the existence of two specific entities is here proposed, which will have impact on conservation policies both in France and in Spain.