Molecular phylogeny and phylogeography of the Cuban cave-fishes of the genus Lucifuga: Evidence for cryptic allopatric diversity

Abstract

Underground environments are increasingly recognized as reservoirs of faunal diversity. Extreme environmental conditions and limited dispersal ability of underground organisms have been acknowledged as important factors promoting divergence between species and conspecific populations. However, in many instances, there is no correlation between genetic divergence and morphological differentiation. Lucifuga Poey is a stygobiotic fish genus that lives in Cuban and Bahamian caves. In Cuba, it offers a unique opportunity to study the influence of habitat fragmentation on the genetic divergence of stygobiotic species and populations. The genus includes four species and one morphological variant that have contrasting geographical distributions. In this study, we first performed a molecular phylogenetic analysis of the Lucifuga Cuban species using mitochondrial and nuclear markers. The mitochondrial phylogeny revealed three deeply divergent clades that were supported by nuclear and morphological characters. Within two of these main clades, we identified five lineages that are candidate cryptic species and a taxonomical synonymy between Lucifuga subterranea and Lucifuga teresinarum. Secondly, phylogeographic analysis using a fragment of the cytochrome b gene was performed for Lucifuga dentata, the most widely distributed species. We found strong geographical organization of the haplotype clades at different geographic scales that can be explained by episodes of dispersal and population expansion followed by population fragmentation and restricted gene flow. At a larger temporal scale, these processes could also explain the diversification and the distribution of the different species.

Evidence for Repeated Loss of Selective Constraint in Rhodopsin of Amblyopsid Cavefishes (Teleostei: Amblyopsidae)

“…Because rhodopsin is located downstream in eye developmental and regulatory cascades (Lamb et al 2007 and references therein), it may become nonfunctional in aphotic environments, as it is released from purifying selection for visual function. However, previous studies examining selective constraint of rhodopsin in subterranean organisms have yet to uncover compelling evidence of loss of functionality at the molecular level (Crandall and Hillis 1997; Janssen et al 2000; Li and He 2009; Zhao et al 2009b; Garcia‐Machado et al 2011; Kim et al 2011). At least 19 genes associated with visual perception were discovered to be lost or showed evidence of LOF constraint in a genome analysis of the naked mole rat (Kim et al 2011); however, rhodopsin was not one of these loci.…”

Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals

“…The sequenced L. gibarensis specimen was a male, had small eyes and was pigmented. All the fish belonging to this species have small eyes whereas their pigmentation is also highly variable (García-Machado, et al 2011). DNA was extracted using a protocol already described elsewhere (García-Machado, et al 2011).…”

“…All the fish belonging to this species have small eyes whereas their pigmentation is also highly variable (García-Machado, et al 2011). DNA was extracted using a protocol already described elsewhere (García-Machado, et al 2011). For L. dentata , paired-end libraries were prepared with different insert sizes: 200 bp, 400 bp and 750 bp.…”

“…In order to examine the long term effect of life in caves on the molecular decay of large sets of genes involved in various light-dependent biological processes, genomes of fishes evolving in caves for a very long time and which did not undergo a recent WGD are required. Two clades of cavefishes (cave brotulas from Bahamas and Cuba) were previously identified in the genus Lucifuga , one comprising only blind cavefish species and the other only small-eyed cavefish species (García-Machado, et al 2011). As no close surface relative has been identified up to now and large genetic distances were found between some species, within and between clades, this genus of cavefishes is likely relatively ancient, and the last common ancestor of extant species was probably a cave-adapted fish.…”

“…The latter species is a new species first identified as Lucifuga sp. 4 (García-Machado, et al 2011) that will be formally named and described in a forthcoming publication.…”