Abstract
BackgroundAquatic subterranean species often exhibit disjunct distributions, with high level of endemism and small range, shaped by vicariance, limited dispersal, and evolutionary rates. We studied the disjunct biogeographic patterns of an endangered blind cave shrimp, Typhlocaris, and identified the geological and evolutionary processes that have shaped its divergence pattern.MethodsWe collected Typlocaris specimens of three species (T. galilea, T. ayyaloni, and T. salentina), originating from subterranean groundwater caves by the Mediterranean Sea, and used three mitochondrial genes (12S, 16S, cytochrome oxygnese subunit 1 (COI)) and four nuclear genes (18S, 28S, internal transcribed spacer, Histon 3) to infer their phylogenetic relationships. Using the radiometric dating of a geological formation (Bira) as a calibration node, we estimated the divergence times of the Typhlocaris species and the molecular evolution rates.ResultsThe multi-locus ML/Bayesian trees of the concatenated seven gene sequences showed that T. salentina (Italy) and T. ayyaloni (Israel) are sister species, both sister to T. galilea (Israel). The divergence time of T. ayyaloni and T. salentina from T. galilea was 7.0 Ma based on Bira calibration. The divergence time of T. ayyaloni from T. salentina was 5.7 (4.4–6.9) Ma according to COI, and 5.8 (3.5–7.2) Ma according to 16S. The computed interspecific evolutionary rates were 0.0077 substitutions/Myr for COI, and 0.0046 substitutions/Myr for 16S.DiscussionTwo consecutive vicariant events have shaped the phylogeographic patterns of Typhlocaris species. First, T. galilea was tectonically isolated from its siblings in the Mediterranean Sea by the arching uplift of the central mountain range of Israel ca. seven Ma. Secondly, T. ayyaloni and T. salentina were stranded and separated by a marine transgression ca. six Ma, occurring just before the Messinian Salinity Crisis. Our estimated molecular evolution rates were in one order of magnitude lower than the rates of closely related crustaceans, as well as of other stygobiont species. We suggest that this slow evolution reflects the ecological conditions prevailing in the highly isolated subterranean water bodies inhabited by Typhlocaris.
Highlights
The biogeographic distribution patterns of populations of aquatic subterranean organisms are characterized by a small range and high degree of endemism, originating from limited dispersal abilities and vicariant events, isolating the subterranean basins (Christman et al, 2005; Culver & Holsinger, 1992; Culver, Pipan & Schneider, 2009; Culver & Sket, 2000; Gibert & Deharveng, 2002; Porter, 2007)
The topology of the five gene phylogenetic tree supports the hypothesis suggesting that T. galilea was separated from its presumed marine ancestor earlier than the separation of T. ayyaloni and T. salentina (H2, Fig. 2)
Our results indicated that two separate vicariant event shaped the distribution patterns of the blind cave-dwelling shrimp Typhlocaris
Summary
The biogeographic distribution patterns of populations of aquatic subterranean organisms (stygobionts) are characterized by a small range and high degree of endemism, originating from limited dispersal abilities and vicariant events, isolating the subterranean basins (Christman et al, 2005; Culver & Holsinger, 1992; Culver, Pipan & Schneider, 2009; Culver & Sket, 2000; Gibert & Deharveng, 2002; Porter, 2007). Among them are at least four crustaceans, found in sites located along the Dead Sea Rift valley with congeneric taxa found in the Mediterranean coastal plain and even in brackish groundwater in the south of Israel These obligate stygobionts are regarded as relicts of extinct marine fauna of ancient Mediterranean transgressions (Por, 1963). Four species of this genus are known from four localities around the east Mediterranean Sea (Fig. 1). Our estimated molecular evolution rates were in one order of magnitude lower than the rates of closely related crustaceans, as well as of other stygobiont species
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