Shotgun Mitogenomics Provides a Reference Phylogenetic Framework and Timescale for Living Xenarthrans

Abstract

Xenarthra (armadillos, sloths, and anteaters) constitutes one of the four major clades of placental mammals. Despite their phylogenetic distinctiveness in mammals, a reference phylogeny is still lacking for the 31 described species. Here we used Illumina shotgun sequencing to assemble 33 new complete mitochondrial genomes, establishing Xenarthra as the first major placental clade to be fully sequenced at the species level for mitogenomes. The resulting data set allowed the reconstruction of a robust phylogenetic framework and timescale that are consistent with previous studies conducted at the genus level using nuclear genes. Incorporating the full species diversity of extant xenarthrans points to a number of inconsistencies in xenarthran systematics and species definition. We propose to split armadillos into two distinct families Dasypodidae (dasypodines) and Chlamyphoridae (euphractines, chlamyphorines, and tolypeutines) to better reflect their ancient divergence, estimated around 42 Ma. Species delimitation within long-nosed armadillos (genus Dasypus) appeared more complex than anticipated, with the discovery of a divergent lineage in French Guiana. Diversification analyses showed Xenarthra to be an ancient clade with a constant diversification rate through time with a species turnover driven by high but constant extinction. We also detected a significant negative correlation between speciation rate and past temperature fluctuations with an increase in speciation rate corresponding to the general cooling observed during the last 15 My. Biogeographic reconstructions identified the tropical rainforest biome of Amazonia and the Guiana Shield as the cradle of xenarthran evolutionary history with subsequent dispersions into more open and dry habitats.

Genome-Wide Screening of Retroviral Envelope Genes in the Nine-Banded Armadillo (Dasypus novemcinctus, Xenarthra) Reveals an Unfixed Chimeric Endogenous Betaretrovirus Using the ASCT2 Receptor

“…Genomic DNA was extracted from the alcohol-preserved livers of the two pregnant females as well as from ear biopsy specimens of other long-nosed armadillo individuals collected in different locations in the United States, Central America (CA), South America, and French Guiana (FG) ( Table 1). Genomic DNAs from Dasypus novemcinc- and Chlamyphorus truncatus were extracted in a previous study (31). Samples used in this study are detailed in Table 1.…”

“…Illumina reads previously produced from low-coverage shotgun genome sequencing of all xenarthran species (31) were also used to test for the presence or absence of DnERV(Env1.1)-related copies. Single reads were mapped onto the sequence of the empty locus, the 5=-LTR and 3=-LTR junctions, and the dasy-Env1.1 ORF by using the medium-sensitivity parameters of the Geneious R9 Mapper (37).…”

“…Remarkably, D. novemcinctus was found to have colonized the southern United States during the last 200 years (32). Moreover, the recent low-coverage shotgun genome sequencing of all xenarthran species allowed a robust phylogenetic framework and time scale to be established (31), thus facilitating the dating of retroviral germ line insertions in this mammalian clade.…”

Mammalian Diversity and Matses Ethnomammalogy in Amazonian Peru Part 2: Xenarthra, Carnivora, Perissodactyla, Artiodactyla, and Sirenia

“…Living armadillos have traditionally been placed in a single family (e.g., by Wilson and Reeder, 2005;Gardner, 2008), but recent phylogenetic results, including the astonishing discovery that glyptodonts are nested within the radiation of Recent armadillos, suggest that Dasypodidae and Chlamyphoridae be recognized as distinct clades of commensurate rank (Gibb et al, 2015;Mitchell et al, 2016). Four armadillo species-two dasypodids and two chlamyphorids-all easily distinguished by salient external and cranial characters (table 2; fig.…”

“…However, it is noteworthy that (1) Amazonian specimens seem to be substantially larger than specimens from other South American landscapes (e.g., the Brazilian highlands and northern Venezuela; Wetzel and Mondolfi, 1979: table 1), (2) sequence variation at the mitochondrial ND1 locus among specimens identified as D. novemcinctus appears to be highly structured geographically (Loughry and McDonough, 2013: fig. 7.2), and (3) phylogenetic analyses of mitogenomes do not recover D. novemcinctus as a monophyletic taxon (Gibb et al, 2015;Mitchell et al, 2016). Unfortunately, western Amazonian populations of D. novemcinctus are not represented in any published molecular analysis.…”