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A subterranean adaptive radiation of amphipods in Europe.

ABSTRACT: 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.

SUBMITTER: Borko S

PROVIDER: S-EPMC8211712 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Mitochondrial genomes play important roles in studying genome evolution, phylogenetic analyses, and species identification. Amphipods (Class Malacostraca, Order Amphipoda) are one of the most ecologically diverse crustacean groups occurring in a diverse array of aquatic and terrestrial environments globally, from freshwater streams and lakes to groundwater aquifers and the deep sea, but we have a limited understanding of how habitat influences the molecular evolution of mitochondrial energy metabolism. Subterranean amphipods likely experience different evolutionary pressures on energy management compared to surface-dwelling taxa that generally encounter higher levels of predation and energy resources and live in more variable environments. In this study, we compared the mitogenomes, including the 13 protein-coding genes involved in the oxidative phosphorylation (OXPHOS) pathway, of surface and subterranean amphipods to uncover potentially different molecular signals of energy metabolism between surface and subterranean environments in this diverse crustacean group. We compared base composition, codon usage, gene order rearrangement, conducted comparative mitogenomic and phylogenomic analyses, and examined evolutionary signals of 35 amphipod mitogenomes representing 13 families, with an emphasis on Crangonyctidae. Mitogenome size, AT content, GC-skew, gene order, uncommon start codons, location of putative control region (CR), length of rrnL and intergenic spacers differed between surface and subterranean amphipods. Among crangonyctid amphipods, the spring-dwelling Crangonyx forbesi exhibited a unique gene order, a long nad5 locus, longer rrnL and rrnS loci, and unconventional start codons. Evidence of directional selection was detected in several protein-encoding genes of the OXPHOS pathway in the mitogenomes of surface amphipods, while a signal of purifying selection was more prominent in subterranean species, which is consistent with the hypothesis that the mitogenome of surface-adapted species has evolved in response to a more energy demanding environment compared to subterranean amphipods. Overall, gene order, locations of non-coding regions, and base-substitution rates points to habitat as an important factor influencing the evolution of amphipod mitogenomes.

Project description:BACKGROUND:Cave organisms have been used as models for evolution and biogeography, as their reduced above-ground dispersal produces phylogenetic patterns of area distribution that largely match the geological history of mountain ranges and cave habitats. Most current hypotheses assume that subterranean lineages arose recently from surface dwelling, dispersive close relatives, but for terrestrial organisms there is scant phylogenetic evidence to support this view. We study here with molecular methods the evolutionary history of a highly diverse assemblage of subterranean beetles in the tribe Leptodirini (Coleoptera, Leiodidae, Cholevinae) in the mountain systems of the Western Mediterranean. RESULTS:Ca. 3.5 KB of sequence information from five mitochondrial and two nuclear gene fragments was obtained for 57 species of Leptodirini and eight outgroups. Phylogenetic analysis was robust to changes in alignment and reconstruction method and revealed strongly supported clades, each of them restricted to a major mountain system in the Iberian peninsula. A molecular clock calibration of the tree using the separation of the Sardinian microplate (at 33 MY) established a rate of 2.0% divergence per MY for five mitochondrial genes (4% for cox1 alone) and dated the nodes separating the main subterranean lineages before the Early Oligocene. The colonisation of the Pyrenean chain, by a lineage not closely related to those found elsewhere in the Iberian peninsula, began soon after the subterranean habitat became available in the Early Oligocene, and progressed from the periphery to the centre. CONCLUSIONS:Our results suggest that by the Early-Mid Oligocene the main lineages of Western Mediterranean Leptodirini had developed all modifications to the subterranean life and were already present in the main geographical areas in which they are found today. The origin of the currently recognised genera can be dated to the Late Oligocene-Miocene, and their diversification can thus be traced to Miocene ancestors fully adapted to subterranean life, with no evidence of extinct epigean, less modified lineages. The close correspondence of organismal evolution and geological record confirms them as an important study system for historical biogeography and molecular evolution.

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A subterranean adaptive radiation of amphipods in Europe.

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