Phylogeographical patterns and a cryptic species provide new insights into Western Indian Ocean giant clams phylogenetic relationships and colonization history

Abstract

Aim: The unique biodiversity in the Red Sea is the result of complex ecological and evolutionary processes driven by Pleistocene climatic change. Here we investigate the species diversity, phylogenetic relationships and phylogeographical patterns of giant clams in the Western Indian Ocean (WIO) and the Red Sea to explore scenarios of marine speciation in this under-studied region. Location: Mozambique Channel, Madagascar, and the Mascarene Islands (WIO); the Farasan Islands (Red Sea). Taxon: Giant clams of the genus Tridacna (Cardiidae: Tridacninae). Methods: Giant clams were sampled as complete organisms or through underwater biopsies. Nuclear (28S) and mitochondrial (16S and COI) DNA sequences were subjected to Bayesian and maximum likelihood analyses to generate a phylogenetic hypothesis for all known species within the genus Tridacna. Bayesian inference with molecular and fossil calibration was used to infer their colonization history. Results: From the 10 genetically distinct clades recovered from the analyses of 253 sequenced specimens, five distinct Tridacna lineages were sampled, three of which were endemics of the WIO and the Red Sea. Each lineage corresponded to a distinct species, except one grouping the two formerly known WIO endemics, T. lorenzi and T. rosewateri. This lineage clustered with two other well-supported lineages: the Red Sea endemic T. squamosina, and a previously unrecognized lineage, restricted to the WIO, for which we resurrect the long-forgotten name T. elongatissima Bianconi, 1856. For the two other species sampled (T. maxima and T. squamosa), contrasting phylogeographical patterns were observed. Main conclusions: Our data confirm the validity of the species T. rosewateri, a WIO endemic genetically indistinguishable from T. lorenzi, which should be considered a junior synonym. The phylogenetic placement of the newly resurrected T. elongatissima provides insights into the probable origin of T. squamosina, which split from its sister species no later than 2 Ma, likely during Middle Pleistocene glacial periods. Two | 1087 FAUVELOT ET AL.

The Small Giant Clam, Tridacna maxima Exhibits Minimal Population Genetic Structure in the Red Sea and Genetic Differentiation From the Gulf of Aden

“…The observed genetic homogeneity inside the Red Sea could be supported by efficient broad scale oceanographic transportation of larvae across the reefs that line the eastern Red Sea and/or a recent colonization with limited time for differentiation. The latter is supported by report of recent colonization of Red Sea T. maxima from the Mozambique channel (Fauvelot et al, 2020). Nevertheless, the genetic homogeneity found in the Red Sea provides a more parsimonious and sufficient explanation, supported by the growing body of literature indicating the importance of the oceanographic features in shaping the genetic structure of marine invertebrate populations.…”

“…During the Pleistocene and the Holocene, the Red Sea experienced a limited gene exchange with the Indian Ocean through the Straits of Bab-el-Mandeb (Siddall et al, 2003), resulting in high levels of endemism among the reef taxa (DiBattista et al, 2016b). Nevertheless, this hypothesized impact of the quaternary period has been argued by a recent study (Fauvelot et al, 2020) suggesting that T. maxima has more recently invaded the Red Sea from the Mozambique Channel. This hypothesis is supported by the discovery of a sister clade between the Red Sea and western Indian Ocean (WIO) populations (i.e., Juan de Nova, Tulear, Reunion Island, and Mauritius) (see Supplementary Figure S2), suggesting that Red Sea giant clams have recently diverged from WIO lineages through synergistic effects of historical and ecological factors (Fauvelot et al, 2020).…”

“…Nevertheless, this hypothesized impact of the quaternary period has been argued by a recent study (Fauvelot et al, 2020) suggesting that T. maxima has more recently invaded the Red Sea from the Mozambique Channel. This hypothesis is supported by the discovery of a sister clade between the Red Sea and western Indian Ocean (WIO) populations (i.e., Juan de Nova, Tulear, Reunion Island, and Mauritius) (see Supplementary Figure S2), suggesting that Red Sea giant clams have recently diverged from WIO lineages through synergistic effects of historical and ecological factors (Fauvelot et al, 2020). Such genetic divergence could be explained by the habitat patchiness of T. maxima between the Gulf of Aden and Kenya (Obura, 2012), creating a restricted steppingstone connectivity between the Red Sea and WIO and thereby increasing the chance for vicariant splits.…”

“…Mitochondrial markers have been found to be suitable to resolve population genetics structures of marine bivalves (Schneider and Ó Foighil, 1999;Mohamed et al, 2006;Richter et al, 2008;Huber and Eschner, 2011;Pappas et al, 2017;Fauvelot et al, 2020), although with limited geographical scope. Previous surveys of Tridacna maxima by Pappas et al (2017) and Othmen et al (2020) were restricted to coral reefs in the northern and central Saudi Arabian Red Sea.…”

Oceanic dispersal barriers in a holoplanktonic gastropod

“…Graves & McDowell, 2015), benthic organisms (e.g. Fauvelot et al., 2020; Prazeres et al., 2020) and other zooplankton (reviewed in Peijnenburg & Goetze, 2013). Based on a strict COI molecular clock rate of 2.4%/million years (MY) for gastropods (Hellberg & Vacquier, 1999), the divergence between the Atlantic and Pacific mitochondrial clades is estimated at ~4.6 MY, which roughly coincides with the emergence of the Isthmus of Panama (Bacon et al., 2015; O'Dea et al., 2016).…”