Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus

Copilaş‐Ciocianu, Denis; Borza, Péter; Petrusek, Adam

doi:10.1016/j.ympev.2017.10.023

Cited by 44 publications

(33 citation statements)

References 110 publications

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“…By contrast, several studies on subterranean beetles (Martins & Ferreira, ; Vergnon et al, ), amphipods from caves (Delić et al, ; Fišer et al, ; Trontelj et al, ; Zakšek, Delić, Fišer, Jalžić, & Trontelj, ), interstitial habitats (Fišer, Delić, Luštrik, Zagmajster, & Altermatt, ) or deep wells (Hutchins, Schwartz, & Nowlin, ), but also spiders (Arnedo, Oromí, Múrria, Macías‐Hernández, & Ribera, ; Mammola, Arnedo, et al, ; Mammola et al, ), suggested that variation in functional traits corresponds to ecological diversification of subterranean species. These studies strongly concur with the results presented here and support the hypothesis that rather than evolutionary dead ends, subterranean organisms continue evolving and actively specializing into new microhabitats (Cieslak, Fresneda, & Ribera, ; Copilaş‐Ciocianu, Fišer, Borza, & Petrusek, ; Stern et al, ).…”

Section: Discussionsupporting

confidence: 90%

Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

et al. 2020

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1. Ecological specialization is an important mechanism enhancing species coexistence within a given community. Yet, unravelling the effect of multiple selective evolutionary and ecological factors leading the process of specialization remains a key challenge in ecology. Subterranean habitats provide highly replicated experimental arenas in which to disentangle the relative contribution of evolutionary history (convergent evolution vs. character displacement) and ecological setting (environmental filtering vs. competitive exclusion) in driving community assembly.2. We tested alternative hypotheses about the emergence of ecological specialization using the radiation of a lineage of sheet-weaver cave-dwelling spiders as model system. We observed that at the local scale, a differential specialization to cave microhabitats generally parallels moderate levels of morphological similarity and close phylogenetic relatedness among species. Conversely, geographic distance contributed little in explaining microhabitat occupation, possibly mirroring a limited role of competitive exclusion. Yet, compared to non-coexisting species, co-occurring species adapted to different microhabitats showed lower morphological niche overlap (i.e. higher dissimilarity) and deeper genetic distance.3. The framework here developed suggests that in the subterranean domain, habitat specialization is primarily driven by environmental filtering, secondarily by convergent evolution, and only marginally by character displacement or competitive exclusion. This pattern results in the establishment of replicated communities across geographical space, composed by ecologically equivalent species. Such process of community assembly well explains the numerous adaptive radiations observed in subterranean habitats, an eco-evolutionary pattern well documented in oceanic islands or mountain summit communities. K E Y W O R D S biotic interactions, cave, functional traits, n-dimensional hypervolume, niche space, phenotypic variability, subterranean biology, Western Italian Alps | 1065 Functional Ecology MAMMOLA et AL. S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Mammola S, Arnedo MA, Fišer C, Cardoso P, Dejanaz AJ, Isaia M. Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders.

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Section: Discussionsupporting

confidence: 90%

Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

et al. 2020

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“…In North-Western Europe, Niphargus colonized freshwater during the Cretaceous, and the Mediterranean clades presumably derived from freshwater ancestors (McInerney et al, 2014). Today, virtually all Niphargus species live in subterranean freshwater, with few exceptions found in anchialine caves (Karaman & Sket, 1989;Sket & Karaman, 1990; but see also Copilaş-Ciocianu, Fišer, Borza, & Petrusek, 2018). The closest relative of Niphargus is the freshwater and anchialine genus Pseudoniphargus (Copilaş-Ciocianu, Borko, & Fišer, 2020;Jurado-Rivera et al, 2017), whereas their putative marine relatives are not known.…”

Section: Introductionmentioning

confidence: 99%

How did subterranean amphipods cross the Adriatic Sea? Phylogenetic evidence for dispersal–vicariance interplay mediated by marine regression–transgression cycles

Delić

Stoch

Borko

et al. 2020

Journal of Biogeography

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Aim Freshwater subterranean amphipods with low dispersal abilities are known from both sides of the impermeable barrier, the Adriatic Sea. We tested the hypothesis that historical marine regression–transgression cycles shaped the distribution patterns of subterranean amphipods through repeated cycles of dispersal and vicariance against the hypothesis that subterranean amphipods colonized both sides of the Adriatic Sea independently. Location Western Balkan Peninsula, Adriatic Sea Islands and Apennine Peninsula, Europe. Taxon Genus Niphargus, a clade of freshwater subterranean amphipods (Crustacea: Amphipoda). Methods The taxonomic structure of the studied clade was revised using unilocus species delimitation methods. The timeframe of cladogenetic events was inferred using a multi‐locus time‐calibrated phylogeny and compared to the main regression–transgression events in the Miocene and Pleistocene. The geographical origin of the studied clade, species range expansions and contractions, as well as vicariance events were assessed through modelling of historical biogeography. Results Subterranean amphipods of the genus Niphargus, found on both sides of the Adriatic Sea, form a monophylum. The reconstructions of ancestral ranges suggest that the clade emerged in the Balkan Peninsula, dispersed three times independently to the Apennine Peninsula and once back to the Balkans. Adriatic Islands were colonized multiple times, predominantly from the Balkan Peninsula. The dispersal–vicariance events correspond to historical regression–transgression cycles in Miocene and Pleistocene. Main conclusions Marine regression–transgression cycles apparently shaped the distribution patterns of subterranean amphipods while the alternative hypothesis received no support. The actual distribution of subterranean faunas apparently reflects old biogeographical events.

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“…Although this scenario is speculative and would need to be tested, we note that cave fishes may be common exceptions to Dollo's law (Collin & Miglietta, 2008), which argues that once a complex trait is lost it is very unlikely to be re-acquired. Although cave-dwellers have been considered evolutionary "dead-ends" (Stern et al,270 2017) owing to their specialization to underground life involving the loss of eyes and pigmentation, evidence from several lineages of organisms adapted to caves including fishes (Dillman et al, 2011), salamanders (Trajano & Cobolli, 2012), scorpions (Prendini et al, 2010), and amphipods (Copilaş-Ciocianu et al, 2018) indicates that reacquisition of surface phenotypes upon recolonization from caves is indeed possible.…”

Section: Discussionmentioning

confidence: 99%

Repeated colonization of caves leads to phenotypic convergence in catfishes (Siluriformes:Trichomycterus) at a small geographical scale

Flórez

Cadena

DoNascimiento

et al. 2020

Preprint

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Across various animal groups, adaptation to the extreme conditions of cave environments has resulted in 15 convergent evolution of morphological, physiological, and behavioral traits. We document a Neotropical cave fish system with ample potential to study questions related to convergent adaptation to cave environments at the population level. In the karstic region of the Andes of Santander, Colombia, cave-dwelling catfishes in the genus Trichomycterus exhibit variable levels of reduction of eyes and body pigmentation relative to surface congeners. We tested whether cave-dwelling, eye reduced, depigmented Trichomycterus from separate caves in Santander 20 were the result of a single event of cave colonization and subsequent dispersal, or of multiple colonizations to caves by surface ancestors followed by phenotypic convergence. Using mitochondrial DNA sequences to reconstruct phylogenetic relationships of Trichomycterus from Santander, we found that caves in this region have been colonized independently by two separate clades. Additional events of cave colonization -and possibly recolonization of surface streams-may have occurred in one of the clades, where surface and cave-dwelling 25 populations exhibit shallow mtDNA differentiation, suggesting recent divergence or divergence in the face of gene flow. We also identified various taxonomic challenges including both a considerable number of potentially undescribed species and likely problems with the circumscription of named taxa. The system appears especially promising for studies on a wide range of ecological and evolutionary questions. 30

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Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus

Cited by 44 publications

References 110 publications

Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

How did subterranean amphipods cross the Adriatic Sea? Phylogenetic evidence for dispersal–vicariance interplay mediated by marine regression–transgression cycles

Repeated colonization of caves leads to phenotypic convergence in catfishes (Siluriformes:Trichomycterus) at a small geographical scale

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