Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): Evidence of discrepant evolutionary traits

Abstract

The species within Xenarthra (sloths, anteaters, and armadillos) are quintessential South American mammals. Of the three groups, Vermilingua (anteaters) contains the fewest extant and paleontological species. Here, we sampled and sequenced the entire mitochondrial genomes (mitogenomes) of two Tamandua species (Tamandua tetradactyla and Tamandua mexicana) (n=74) from Central and South America, as well as Myrmecophaga tridactyla (n=41) from South America. Within Tamandua, we detected three different haplogroups. The oldest (THI) contained many specimens with the T. tetradactyla morphotype (but also several with the T. mexicana morphotype) and originated in southeastern South America (currently Uruguay) before moving towards northern South America, where the THII haplogroup originated. THII primarily contained specimens with the T. mexicana morphotype (but also several with the T. tetradactyla morphotype) and was distributed in Central America, Colombia, and Ecuador. THI and THII yielded a genetic distance of 4%. THII originated in either northern South America or “in situ” in Central America with haplogroup THIII, which consisted of ~50% T. mexicana and 50% T. tetradactyla phenotypes. THIII was mostly located in the same areas as THII, i.e., Central America, Ecuador, and Colombia, though mainly in the latter. The three haplogroups overlapped in Colombia and Ecuador. Thus, T. tetradactyla and T. mexicana were not reciprocally monophyletic. For this reason, we considered that a unique species of Tamandua likely exists, i.e., T. tetradactyla. In contrast to Tamandua, M. tridactyla did not show different morphotypes throughout its geographical range in the Neotropics. However, two very divergent genetic haplogroups (MHI and MHII), with a genetic distance of ~10%, were detected. The basal haplogroup, MHI, originated in northwestern South America, whereas the more geographically derived haplogroup, MHII, overlapped with MHI, but also expanded into central and southern South America. Thus, Tamandua migrated from south to north whereas Myrmecophaga migrated from north to south. Our results also showed that temporal mitochondrial diversification for Tamandua began during the Late Pliocene and Upper Pleistocene, but for Myrmecophaga began during the Late Miocene. Furthermore, both taxa showed elevated levels of mitochondrial genetic diversity. Tamandua showed more evidence of female population expansion than Myrmecophaga. Tamandua experienced population expansion ~0.6-0.17 million years ago (Mya), whereas Myrmecophaga showed possible population expansion ~0.3-0.2 Mya. However, both taxa experienced a conspicuous female decline in the last 10 000-20 000 years. Our results also showed little spatial genetic structure for both taxa. However, several analyses revealed higher spatial structure in Tamandua than in Myrmecophaga. Therefore, Tamandua and Myrmecophaga were not subjected to the same biogeographical, geological, or climatological events in shaping their genetic structures.