Rodents of the Caribbean: origin and diversification of hutias unravelled by next-generation museomics

Abstract

The Capromyidae (hutias) are endemic rodents of the Caribbean and represent a model of dispersal for non-flying mammals in the Greater Antilles. This family has experienced severe extinctions during the Holocene and its phylogenetic affinities with respect to other caviomorph relatives are still debated as morphological and molecular data disagree. We used target enrichment and next-generation sequencing of mitochondrial and nuclear genes to infer the phylogenetic relationships of hutias, estimate their divergence ages, and understand their mode of dispersal in the Greater Antilles. We found that Capromyidae are nested within Echimyidae (spiny rats) and should be considered a subfamily thereof. We estimated that the split between hutias and Atlantic Forest spiny rats occurred 16.5 (14.8-18.2) million years ago (Ma), which is more recent than the GAARlandia land bridge hypothesis (34)(35). This would suggest that during the Early Miocene, an echimyid-like ancestor colonized the Greater Antilles from an eastern South American source population via rafting. The basal divergence of the Hispaniolan Plagiodontia provides further support for a vicariant separation between Hispaniolan and western islands (Bahamas, Cuba, Jamaica) hutias. Recent divergences among these western hutias suggest Plio-Pleistocene dispersal waves associated with glacial cycles.

Contrasting Phylogenetic and Diversity Patterns in Octodontoid Rodents and a New Definition of the Family Abrocomidae

“…4; Appendix). The relationships among echimyids are mostly in agreement with previous molecular (Galewski et al 2005;Upham and Patterson 2012, in press;Upham et al 2013;Fabre et al 2013Fabre et al , 2014Loss et al 2014), morphological (Emmons 2005;Olivares et al 2012;Candela and Rasia 2012;Verzi et al 2014), and combined phylogenies Verzi et al 2015). Although with some differences, especially in the arrangement of the arboreal genera, these results are consistent in recovering two major subclades, one formed by the terrestrial spiny rat Trinomys plus the fossorial genera, and the other, by terrestrial and arboreal spiny rats, and the semiaquatic coypu (although see Candela and Rasia 2012).…”

Herbarium genomics: skimming and plastomics from archival specimens

“…All in all the term 'museomics' , i.e. the large-scale analysis of the DNA content of museum collections, has become established in several research programmes (Gushanski et al 2013;Fabre et al 2014;Chomicki and Renner 2015;Der Sarkissian et al 2015), in addition to 'palaeogenomics' (Hofreiter et al 2015) where the age of specimens and their DNA extends to beyond neolithic times. And when ancient DNA is no longer present, ancient protein sequences have proven successful instead, for instance to resolve phylogenetic relationships of Late Quaternary South American ungulates (Welker et al 2015).…”

“…Since its application to archival DNA, second-generation sequencing has yielded spectacular results, with, e.g. discovering new hominids from sequencing of small bone fragments (Reich et al 2010), sequencing genomes from extinct lineages such as the Tasmanian tiger (Miller et al 2009), or placing Caribbean endemic lineages of rodent (Fabre et al 2014). Malaspinas (2016) summarized methods to characterize selective sweeps using ancient DNA time-series samples, opening up a fascinating field of research.…”

A Review of thePattonomys/ToromysClade (Rodentia: Echimyidae), with Descriptions of a NewToromysSpecies and a New Genus

“…Recent morphological (Emmons, 2005) and molecular inferences (Galewski et al, 2005;Fabre et al, 2013Fabre et al, , 2014Fabre et al, , 2016bUpham et al, 2013;Upham and Patterson, 2015) have elucidated the longstanding enigma of the deep relationships among many genera of Echimyidae, and resolved some thorny phylogenetic questions with robust and well-supported hypotheses that both disentangled their phylogenetic histories and recovered unexpected relationships, such as the placement of the painted tree rat Callistomys pictus (Pictet, 1843) within Myocastorini (Loss et al, 2014;Fabre et al, 2016b). The clade Echimyini (sensu Fabre et al, 2016b) includes 13 of the 18 described genera of the Echimyinae in a radiation associated with an arboreal lifestyle, and it encompasses much of echimyid morphological diversity (Monteiro et al, 2005;Emmons et al, 2015a;Fabre et al, 2016aFabre et al, , 2016b, with striking ecomorphs such as the bamboo rats (Dactylomys, Kannabateomys, and Olallamys species) and the red-crested tree rat (Santamartamys rufodorsalis).…”