Adaptive radiations are bursts of evolutionary species diversification that have contributed to much of the species diversity on Earth. An exception is modern Europe, where descendants of ancient ...adaptive radiations went extinct, and extant adaptive radiations are small, recent and narrowly confined. However, not all legacy of old radiations has been lost. Subterranean environments, which are dark and food-deprived, yet buffered from climate change, have preserved ancient lineages. Here we provide evidence of an entirely subterranean adaptive radiation of the amphipod genus Niphargus, counting hundreds of species. Our modelling of lineage diversification and evolution of morphological and ecological traits using a time-calibrated multilocus phylogeny suggests a major adaptive radiation, comprised of multiple subordinate adaptive radiations. Their spatio-temporal origin coincides with the uplift of carbonate massifs in South-Eastern Europe 15 million years ago. Emerging subterranean environments likely provided unoccupied, predator-free space, constituting ecological opportunity, a key trigger of adaptive radiation. This discovery sheds new light on the biodiversity of Europe.
Current theory predicts that a shift to a new habitat would increase the rate of diversification, while as lineages evolve into multiple species, intensified competition would decrease the rate of ...diversification. We used Holarctic amphipods of the genus Gammarus to test this hypothesis. We sequenced four genes (5,088 bp) for 289 samples representing 115 Gammarus species. A phylogenetic analysis showed that Gammarus originated from the Tethyan region with a saline ancestry in the Paleocene, and later colonized the freshwater habitat in the Middle Eocene. Ancestral range reconstruction and diversification mode analysis combined with paleogeological and paleoclimatic evidence suggested that the habitat shift from saline to freshwater led to an increased diversification rate. The saline lineage of Gammarus dispersed to both sides of the Atlantic at 55 million years ago (Ma), because of the few barriers between the Tethys and the Atlantic, and diversified throughout its evolutionary history with a constant diversification rate 0.04 species per million years (sp/My). The freshwater Gammarus, however, underwent a rapid diversification phase (0.11 sp/My) until the Middle Miocene, and lineages successively diversified across Eurasia via vicariance process likely driven by changes of the Tethys and landmass. In particular, the freshwater Gammarus lacustris and Gammarus balcanicus lineages had a relatively high diversification shift, corresponding to the regression of the Paratethys Sea and the continentalization of Eurasian lands during the Miocene period. Subsequently (14 Ma), the diversification rate of the freshwater Gammarus decreased to 0.05 and again to 0.01 sp/My. The genus Gammarus provides an excellent aquatic case supporting the hypothesis that ecological opportunities promote diversification.
Recent studies indicate that morphologically cryptic species may be ecologically more different than would be predicted from their morphological similarity and phylogenetic relatedness. However, in ...biodiversity research it often remains unclear whether cryptic species should be treated as ecologically equivalent, or whether detected differences have ecological significance. In this study, we assessed the ecological equivalence of four morphologically cryptic species of the amphipod genus Niphargus. All species live in a small, isolated area on the Istrian Peninsula in the NW Balkans. The distributional ranges of the species are partially overlapping and all species are living in springs. We reconstructed their ecological niches using morphological traits related to feeding, bioclimatic niche envelope and species' preference for epi-hypogean habitats. The ecological meaning of differences in niches was evaluated using distributional data and co-occurrence frequencies. We show that the species comprise two pairs of sister species. All species differ from each other and the degree of differentiation is not related to phylogenetic relatedness. Moreover, low co-occurrence frequencies in sympatric zones imply present or past interspecific competition. This pattern suggests that species are not differentiated enough to reduce interspecific competition, nor ecologically equivalent to co-exist via neutral dynamics. We tentatively conclude that the question of ecological equivalence relates to the scale of the study: at a fine scale, species' differences may influence dynamics in a local community, whereas at the regional level these species likely play roughly similar ecological roles.
Secondary salinization of freshwater is becoming a growing environmental problem. Currently, there is few data available on the effects of salinisation on subterranean crustaceans that are vital for ...the maintenance of groundwater ecosystem functioning. In this study, the sensitivity of subterranean Niphargus amphipods to NaCl was investigated. We expected that cave-dwelling species would be more sensitive as surface-subterranean boundary species. Eight ecologically different Niphargus species were tested: four live at the boundary between the surface and subterranean ecosystems (N. timavi, N. krameri, N. sphagnicolus, N. spinulifemur), three live in cave streams (N. stygius, N. scopicauda, N. podpecanus), and one species (N. hebereri) lives in anchialine caves and wells. The organisms were exposed to five concentrations of NaCl for 96 h and afterwards the immobility, mortality, and electron transfer system (ETS) activity (a measure for metabolic rate of animals) were evaluated. As expected, the most tolerant species was N. hebereri dwelling in naturally high-salinity habitat. However, contrary to our expectations, the species collected at the surface-subterranean boundary were more sensitive as cave stream species when their immobility and mortality were assessed. Interestingly, the majority of Niphargus tested were more NaCl tolerant as can be deduced from currently available data for subterranean and surface crustaceans. We could not observe a clear trend in ETS activity changes between groups of surface-subterranean boundary and cave streams species after exposure to NaCl stress, but it appears that osmotic stress-induced metabolic rate changes are species-specific. This study shows that amphipods Niphargus can be a valuable subterranean environmental research model and further ecotoxicity research is of interest.
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•Eight subterranean Niphargus amphipod species exhibit differential sensitivity to salinity.•Surface-subterranean boundary species are more sensitive as cave stream species.•The majority of Niphargus tested are more NaCl tolerant as reported for other crustaceans.•Metabolic rate changes upon NaCl exposure are species-specific and not related to Niphargus habitat.•Niphargus amphipods are valuable ecotoxicity test species.
In light of recent alarming trends in human population growth, climate change, and other environmental modifications, a “Warning to humanity” manifesto was published in BioScience in 2017. This call ...reiterated most of the ideas originally expressed by the Union of Concerned Scientists in 1992, including the fear that we are “pushing Earth’s ecosystems beyond their capacities to support the web of life.” As subterranean biologists, we take this opportunity to emphasize the global importance and the conservation challenges associated with subterranean ecosystems. They likely represent the most widespread nonmarine environments on Earth, but specialized subterranean organisms remain among the least documented and studied. Largely overlooked in conservation policies, subterranean habitats play a critical role in the function of the web of life and provide important ecosystem services. We highlight the main threats to subterranean ecosystems and propose a set of effective actions to protect this globally important natural heritage.
Species that successfully colonized subterranean environments are subject to two opposing selection processes. Stringent abiotic factors select for convergent adaptations, such as loss of eyes and ...pigments, while interspecific competition drives between‐species divergence. Subterranean species can resolve opposing selection by adaptation to physically different microhabitats. Yet, species frequently co‐occur in physically homogeneous subterranean habitats, like interstitial. These co‐occurrences in such a narrow ecological context can be explained either by equalizing mechanisms, in which neither of the co‐occurring species has a competitive advantage, or by more complex niche models that include species’ differentiation along a trophic niche axis. We tested these hypotheses using the amphipod genus Niphargus. We analysed Europe‐wide co‐occurrence records of Niphargus species from interstitial habitats, split into six independent large‐scale regions. Firstly, we addressed whether species’ pairwise co‐occurrences are random using a probabilistic model. Secondly, we tested whether species cluster into distinct functional–morphological groups and whether ecologically or phylogenetically distinct species are more likely to co‐occur. We found that 68% of species co‐occurrences were not different from random expectation, indicating that most species had access to most sites within each region. The remaining 32% co‐occurred either significantly more or less often than expected by chance. Cluster analysis of functional morphological characters showed that interstitial species belong to two feeding types, micro‐ and macrofeeders, likely representing two peaks of the interstitial adaptive landscape, and hinting that niche divergence, as a mechanism allowing coexistence, is favoured. Finally, we found that the number of co‐occurrences increases with increasing differentiation of functional morphology, but not phylogenetic differences. We conclude that ecological differentiation may be important in shaping such interstitial communities.
Studying parallel evolution (repeated, independent evolution of similar phenotypes in similar environments) is a powerful tool to understand environment‐dependent selective forces. Surface‐dwelling ...species that repeatedly and independently colonized caves provide unique models for such studies. The primarily surface‐dwelling Asellus aquaticus species complex is a good candidate to carry out such research, because it colonized several caves in Europe. By comparing 17 functional morphological traits between six cave and nine surface populations of the A. aquaticus species complex, we investigated population divergence in morphology and sexual dimorphism. We found habitat‐dependent population divergence in 10 out of 17 traits, likely reflecting habitat‐driven changes in selection acting on sensory systems, feeding, grooming, and antipredator mechanisms. Sexual dimorphism was present in 15 traits, explained by sexual selection acting on male traits important in male–male agonistic behavior or mate guarding and fecundity selection acting on female traits affecting offspring number and nursing. In eight traits, the degree of sexual dimorphism was habitat dependent. We conclude that cave‐related morphological changes are highly trait‐ and function‐specific and that the strength of sexual/fecundity selection strongly differs between cave and surface habitats. The considerable population variation within habitat type warrants further studies to reveal cave‐specific adaptations besides the parallel patterns.
Surface‐dwelling species that repeatedly and independently colonized caves such as Asellus aquaticus provide unique models to study parallel evolution. We measured and analyzed 17 functional morphological traits on 656 individuals from 15 cave and surface populations. We found that besides the expected habitat‐related morphological changes habitat type also affected sexual dimorphism.
1. Various groundwater habitats have exceptionally high levels of endemism caused by strong hydrographical isolation and low dispersal abilities of their inhabitants. More than 10% of ...macro-stygobiotic species nevertheless occupy relatively large ranges, measuring from some hundred to over 2000 km in length. These species represent a challenge because their distributions disregard hydrographical boundaries, and their means to disperse and maintain long-term gene flow are unknown. 2. Based on mitochondrial and nuclear gene sequences, we examined the phylogeographic structure of six formally recognised stygobiotic species (Niphargus virei, N. rhenorhodanensis, Troglocaris anophthalmus, T. hercegovinensis, Spelaeocaris pretneri, Proteus anguinus) and searched for cryptic lineage diversity in a genus-wide phylogeny of Niphargus. Using tree-based criteria as well as comparative divergence measures, we identified cryptic lineages, which may tentatively be equated with cryptic species. 3. Fourteen analysed nominal stygobiotic species with large ranges emerged as highly diversified, splitting into 51 tentative cryptic lineages. The degree of divergence was within the range or larger than the divergence of other related pairs of sister species. A substantial part (94%) of the cryptic lineages had ranges <200 km in length. One half of them were recorded at single sites only. The largest range recorded was that of a cryptic N. virei lineage (700 km), while none of the very large traditional ranges (e.g. Niphargus aquilex- 2300 km, N. tauri- 1900 km) could be corroborated. 4. These data suggest that small ranges of macro-stygobionts are the rule, and ranges over 200 km are extremely rare. 5. The implications of this result for groundwater biodiversity assessment and conservation include a considerable increase in overall diversity at the regional and continental scale and a strong decrease in faunal similarities among regions, coupled with greater endemism.
Climate change affects all ecosystems, but subterranean ecosystems are repeatedly neglected from political and public agendas. Cave habitats are home to unknown and endangered species, with low trait ...variability and intrinsic vulnerability to recover from human-induced disturbances. We studied the annual variability and cyclicity of temperatures in caves vis-à-vis surface in different climatic areas. We hypothesize that cave temperatures follow the average temperature pattern at the surface for each location with a slight delay in the signal, but we found three different thermal patterns occurring in caves: (1) high positive correlation and a similar thermal pattern to the surface, (2) low correlation and a slight thermal delay of the signal from the surface, and (3) high negative correlation with an extreme delay from the surface. We found daily thermal cycles in some caves, which may potentially control the circadian rhythms of cave organisms. Our results show that caves had lower thermal amplitude than the surface, and that thermal averages within caves approximately correspond to the to the annual average of surface temperature. Caves buffer external temperature and act as refugia for biota in extreme climatic events. Likewise, temperature increases at surface will lead to increment in caves, threatening subterranean biota and ecosystem services.
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