Diversity of the Southeast Asian leaf turtle genus Cyclemys: how many leaves on its tree of life?

Abstract

In the present study, we use mtDNA sequence data (cyt b gene) in combination with nuclear DNA sequences (C‐mos, Rag2 genes, R35 intron), nuclear genomic fingerprints (ISSR) and morphological data to reveal species diversity within the Southeast Asian leaf turtle genus Cyclemys, a morphologically difficult group comprising cryptic species. Two morphologically distinct major groupings exist, a yellow‐bellied species group with three taxa (Cyclemys atripons, C. dentata, C. pulchristriata) and a dark‐bellied species group. The latter contains besides the morphologically variable C. oldhamii three additional new species (C. enigmatica n. sp., C. fusca n. sp., C. gemeli n. sp.). According to mtDNA data, C. fusca and C. gemeli constitute with high support the sister group of a clade comprising all other species, indicating that the dark‐bellied species are not monophyletic, despite morphological similarity. mtDNA sequences of C. enigmatica, being highly distinct in nuclear genomic markers, do not differ from the sympatric C. dentata, suggesting that the original mitochondrial genome of C. enigmatica was lost due to introgressive hybridization. Morphological discrimination of Cyclemys species is possible using multivariate methods. However, gross morphology of most dark‐bellied species on the one hand and of C. atripons and C. pulchristriata on the other is so similar that reliable species determination is only possible when genetic markers are used. The high diversity within Cyclemys requires revision of the IUCN Red List Categories for leaf turtles because the former assessment was based on the wrong assumption that in the entire range of the genus occurs only a single species.

Mitochondrial variation among Australian freshwater turtles (genus Myuchelys), with special reference to the Endangered M. bellii

“…Failure to recognise underlying cryptic diversity at or below the level of species can have a great influence on biological conservation outcomes, either through declines in cryptic species that go undetected and as a result are poorly managed (as with Cyclemys; Fritz et al 2008, Stuart & Fritz 2008 or because diversity that is suspected but with poor foundation leads to misallocation of resources (Georges et al 2011). In addition, phylogenetic information has a role to play in assessing distinctiveness, an attribute that has an influence on determining conservation priorities (Faith 1992, Moritz 1995.…”

Complex phylogeography in Rhinoclemmys melanosterna: conflicting mitochondrial and nuclear evidence suggests past hybridization (Testudines: Geoemydidae)

“…This is especially true for species occurring in the Neotropics (Central and South America), where relatively few phylogeographic studies have been performed so far (for a review see Vargas-Ramírez et al 2012a). Such studies are crucial for unravelling evolutionarily significant units (Moritz 1994) that may correspond to unrecognized taxa or cryptic species (for chelonians, e.g., Fritz et al 2005Fritz et al , 2008Fritz et al , 2011Fritz et al , 2012aPraschag et al 2007Praschag et al , 2011Vargas-Ramírez et al 2010; and have relevance for conservation. Moreover, such investigations elucidate underlying historical events and processes that may have shaped the current genetic diversity (e.g., Vargas-Ramírez et al 2010Fritz et al 2012b, c).…”

Complete mitochondrial genome of the Cyclemys dentata and phylogenetic analysis of the major family Geoemydidae

“…In our study, C. dentata and C. atripons were clustered together, indicating that they are sister species. Fritz et al (2008) found that the mtDNA sequences of C. enigmatica did not differ from those of C. dentata but were highly distinct with regard to nuclear genomic markers, suggesting that the original mt genome of C. enigmatica was lost due to introgressive hybridization . Hybridization among species might lead to a loss in biodiversity within the genus Cyclemys.…”

“…Leaf turtles (genus Cyclemys, Geoemydidae) (Bell, 1834) were previously thought to belong to a genus that included only one or 2 species (Iverson, 1992); later, additional species were identified (Guicking et al, 2002;Fritz et al, 1997Fritz et al, , 2008Stuart and Fritz, 2008). According to morphology and preliminary nuclear DNA data, the Cyclemys could have 6 species, including 2 morphologically distinct groups, a yellow-bellied species group (C. dentata, C. atripons, and C. pulchristriata) and a dark-bellied species group (C. enigmatica, C. fusca, and C. gemeli) .…”

“…Because of its maternal inheritance, relative lack of recombination, and a higher rate of base substitution than most nuclear genes, the mt genome has been widely used to study taxonomy, phylogeny, genetic structure, and biological identification (Jiang et al, 2011). It has been employed as a marker in turtle science (Avise et al, 1992;Bowen et al, 1994;Shaffer et al, 1997;Kumazawa and Nishida 1999;Cao et al, 2000;van der Kuyl et al, 2002;Spinks et al, 2004;Krenz et al, 2005;Parham et al, 2006;Fritz et al, 2008;Stuart and Fritz, 2008;Zhang et al, 2008b;Wiens et al, 2010).…”