Extensive Morphological Convergence and Rapid Radiation in the Evolutionary History of the Family Geoemydidae (Old World Pond Turtles) Revealed by SINE Insertion Analysis

Abstract

The family Geoemydidae is one of three in the superfamily Testudinoidea and is the most diversified family of extant turtle species. The phylogenetic relationships in this family and among related families have been vigorously investigated from both morphological and molecular viewpoints. The evolutionary history of Geoemydidae, however, remains controversial. Therefore, to elucidate the phylogenetic relationships of Geoemydidae and related species, we applied the SINE insertion method to investigate 49 informative SINE loci in 28 species. We detected four major evolutionary lineages (Testudinidae, Batagur group, Siebenrockiella group, and Geoemyda group) in the clade Testuguria (a clade of Geoemydidae + Testudinidae). All five specimens of Testudinidae form a monophyletic clade. The Batagur group comprises five batagurines. The Siebenrockiella group has one species, Siebenrockiella crassicollis. The Geoemyda group comprises 15 geoemydines (including three former batagurines, Mauremys reevesii, Mauremys sinensis, and Heosemys annandalii). Among these four groups, the SINE insertion patterns were inconsistent at four loci, suggesting that an ancestral species of Testuguria radiated and rapidly diverged into the four lineages during the initial stage of its evolution. Furthermore, within the Geoemyda group we identified three evolutionary lineages, namely Mauremys, Cuora, and Heosemys. The Heosemys lineage comprises Heosemys, Sacalia, Notochelys, and Melanochelys species, and its monophyly is a novel assemblage in Geoemydidae. Our SINE phylogenetic tree demonstrates extensive convergent morphological evolution between the Batagur group and the three species of the Geoemyda group, M. reevesii, M. sinensis, and H. annandalii.

Transposable Elements in Reptilian and Avian (Sauropsida) Genomes

“…Short interspersed elements (SINEs) are one of the major types of mobile elements in vertebrate genomes and are generally lineage-specific [Ohshima and Okada, 2005]. SINEs are among the first retroposons to be very extensively studied in sauropsid genomes [Endoh and Okada, 1986;Endoh et al, 1990;Smit and Riggs, 1995;Ohshima et al, 1996;Okada et al, 1997;Terai et al, 1998;Gilbert and Labuda, 1999;Fantaccione et al, 2004;Sasaki et al, 2004;Bejerano et al, 2006;Kosushkin et al, 2006Kosushkin et al, , 2008Nishihara et al, 2006;Piskurek et al, 2006Piskurek et al, , 2009Sasaki et al, 2006;Piskurek and Okada, 2007;Shedlock et al, 2007;Gogolevsky et al, 2008;Hirakawa et al, 2009]. The first sauropsid SINE to be discovered was polIII/SINE in turtles [Endoh and Okada, 1986;Endoh et al, 1990], and its LINE partner is CR1 LINE [Ohshima et al, 1996;Kajikawa et al, 1997].…”

A new species of the genus <i>Ocadia</i> (Testudines: Geoemydidae) from the middle Miocene of Tanegashima Island, southwestern Japan and its paleogeographic implications

“…This presumption appears to be very unlikely because it was deduced from the hypothesis that the genus Ocadia is allied to the "Batagur complex" (McDowell 1964) consisting of Batagur baska sensu lato, B. borneoensis, Chinemys, Heosemys annandalii, Malayemys, and Ocadia. However, recent molecular phylogenetic analyses showed that the "Batagur complex" is not monophyletic (e.g., Barth et al 2004;Spinks et al 2004;Sasaki et al 2006). This suggests that O. tanegashimensis from the Kawachi Formation may have been transported from a nearby lowland area via a river.…”

“…Recent molecular phylogenetic analyses have shown that the genus Ocadia is included in a clade with Chinemys spp. and Mauremys japonica and that these taxa form another more inclusive clade with the remaining living species of Mauremys (Mauremys sensu lato, Honda et al 2002;Barth et al 2004;Feldman and Parham 2004;Spinks et al 2004;Sasaki et al 2006;Jiang et al 2011). However, no synapomorphic morphological character states are known for the two clades (e.g., Honda et al 2002;Hirayama et al 2007).…”

“…In recent molecular phylogenetic studies, this genus has been frequently synonymized with Mauremys along with Chinemys (e.g., Fritz and Havaš 2007;Turtle Taxonomy Working Group 2007;Lovich et al 2011) because O. sinensis, M. japonica and Chinemys spp. form a monophyletic clade and are included in a major, more inclusive clade with the other species of the genus Mauremys sensu stricto (Honda et al 2002;Barth et al 2004;Feldman and Parham 2004;Spinks et al 2004;Sasaki et al 2006;Jiang et al 2011). However, to date, no diagnostic morphological features or synapomorphies are known for the clade embracing O. sinensis, M. japonica, and Chinemys spp.…”

Mauremys reevesii (Gray 1831) – Reeves' Turtle, Chinese Three-Keeled Pond Turtle

“…Shaffer et al (1997) used a combination of molecular and morphological data to suggest a possible close affinity of Chinemys with Heosemys. Moreover, more recent molecular studies have yielded phylogenetic trees on which Chinemys, as well as the genus Ocadia, are consistently located within a cluster with the genus Mauremys (Wu et al 1998;McCord et al 2000;Honda et al 2002;Barth et al 2004;Spinks et al 2004;Feldman and Parham 2004;Sasaki et al 2006;Jiang et al 2011). In contrast, Parham et al (2001) presented a phylogenetic hypothesis based on molecular data where C. reevesii and C. nigricans were clearly separated from Mauremys species recognized at that date.…”