Genetic differentiation between cave and surface-dwelling populations of Garra barreimiae (Cyprinidae) in Oman

Abstract

BackgroundPhenotypic similarities among cave-dwelling animals displaying troglomorphic characters (e.g. reduced eyes and lack of pigmentation) have induced a long-term discussion about the forces driving convergent evolution. Here we introduce Garra barreimiae Fowler & Steinitz, 1956, as an interesting system to study the evolution of troglomorphic characters. The only hitherto known troglomorphic population of this species lives in Al Hoota Cave (Sultanate of Oman) close to a surface population. As a first approach, we assessed the genetic differentiation between the two morphotypes of G. barreimiae to determine whether gene flow still occurs.ResultsWe analysed the mitochondrial control region (CR). In G. barreimiae the CR starts immediately downstream of the tRNA-Thr gene, while the tRNA-Pro gene is missing at this genomic location. Interestingly, a putative tRNA-Pro sequence is found within the CR. The phylogenetic analyses of the CR sequences yielded a tree divided into three clades: Clade 1 has a high genetic distance to the other clades and contains the individuals of three populations which are separated by a watershed from all the others. Clade 2 comprises the individuals from Wadi Bani Khalid, the geographically most remote population. Clade 3 comprises all other populations investigated including that of Al Hoota Cave. The latter forms a haplogroup which also includes individuals from the adjacent surface population.ConclusionsOur data indicates that the troglomorphic cave population is of quite recent origin supporting the hypothesis that selection drives the fast evolution of troglomorphic traits. In this context pleiotropic effects might play an important role as it has been shown for Astyanax. There seems to be some gene flow from the cave population into the adjacent surface populations. One blind individual, found at a surface locality geographically distinct from Al Hoota Cave, is genetically differentiated from the other blind specimens indicating the probable existence of another cave population of G. barreimiae. The phylogeographic analyses show that while some of the surface populations are either still in contact or have been until recently, the population Wadi Bani Khalid is genetically separated. One group consisting of three populations is genetically highly differentiated questioning the conspecifity with G. barreimiae.

Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization

“…However, Kruckenhauser et al (2011) estimated a split below 1 Myr between the two forms of G. barreimiae, and their experiments indicate that the sequences of the cytb gene used by Colli et al (2008) may be derived partly from the functional cytb gene and partly from nuclear pseudogenes (numts (copies of mitochondrial genes that have been translocated into the nuclear genome)). For this reason, in the present study we resequenced the cytb gene in both G. barreimiae and P. andruzzii cavefish and analyzed this together with cytb sequences from an additional 146 species ( Supplementary Figures 1 and 2).…”

“…To address the question of whether other light-related mechanisms are also undergoing degeneration, we also tested for a change in the rate of evolution on the visual receptor rhodopsin (rho) that is expressed in the brain of P. andruzzii, is still functional and is probably involved in photophobic behavior (Tarttelin et al, 2012). These gene sequences were also analyzed in another blind cavefish, Garra barremiae, from Oman that much more recently colonized subterranean waters and evolved troglomorphic traits (Kruckenhauser et al, 2011). The two cavefish show an extremely similar osteology (Banister, 1984), and a recent phylogenetic study proposed that Phreatichthys should be treated as a junior synonym of Garra (Yang et al, 2012).…”

“…The P. andruzzii and G. barreimiae individuals typed in this study are described in Table 1 (Berti and Messana, 2010;Kruckenhauser et al, 2011).…”

“…As a consequence of increases in North East African aridity after 2.8 Myr that led to the desertification at the surface (deMenocal, 1995), P. andruzzii ancestors that colonized the cave environment remained isolated in the dark of the phreatic waters. This complete isolation is because of the disappearance of surface populations, unlike some other species that maintain some level of gene flow with surface-dwelling populations (Li and He, 2009;Kruckenhauser et al, 2011). The extent to which gene flow occurs between surface-and cave-dwelling forms is still debated for A. mexicanus, the model species in cavefish evolution (Bradic et al, 2012;Gross, 2012;Strecker et al, 2012).…”

The morphological diversity of Garra barreimiae [Teleostei: Cyprinidae]

“…In 1980 Dunsire and Gallagher reported a subterranean population of G. barreimiae from the Al Hoota Cave close to Nizwa (Banister 1984). This troglomorphic population seems to be of recent origin less than one million years ago (Kruckenhauser et al 2011), however occasional gene flow between the cave population and the surface population seems to take place (Kirchner et al 2017). Although many populations of G. barreimiae are very isolated from each other and inhabit different drainage systems around the Hajar Mountains (Kruckenhauser et al 2011;Freyhof et al 2015), in former times during intermittent pluvial intervals, the river network was much denser, so populations might have been more connected.…”