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Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation.

ABSTRACT: Identifying general patterns of colonization and radiation in island faunas is often hindered by past human-caused extinctions. The insular Caribbean is one of the only complex oceanic-type island systems colonized by land mammals, but has witnessed the globally highest level of mammalian extinction during the Holocene. Using ancient DNA analysis, we reconstruct the evolutionary history of one of the Caribbean's now-extinct major mammal groups, the insular radiation of oryzomyine rice rats. Despite the significant problems of recovering DNA from prehistoric tropical archaeological material, it was possible to identify two discrete Late Miocene colonizations of the main Lesser Antillean island chain from mainland South America by oryzomyine lineages that were only distantly related. A high level of phylogenetic diversification was observed within oryzomyines across the Lesser Antilles, even between allopatric populations on the same island bank. The timing of oryzomyine colonization is closely similar to the age of several other Caribbean vertebrate taxa, suggesting that geomorphological conditions during the Late Miocene facilitated broadly simultaneous overwater waif dispersal of many South American lineages to the Lesser Antilles. These data provide an important baseline by which to further develop the Caribbean as a unique workshop for studying island evolution.

SUBMITTER: Brace S

PROVIDER: S-EPMC4424637 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation.

Brace Selina S Turvey Samuel T ST Weksler Marcelo M Hoogland Menno L P ML Barnes Ian I

Proceedings. Biological sciences 20150501 1807

Identifying general patterns of colonization and radiation in island faunas is often hindered by past human-caused extinctions. The insular Caribbean is one of the only complex oceanic-type island systems colonized by land mammals, but has witnessed the globally highest level of mammalian extinction during the Holocene. Using ancient DNA analysis, we reconstruct the evolutionary history of one of the Caribbean's now-extinct major mammal groups, the insular radiation of oryzomyine rice rats. Desp ...[more]

PMID: 25904660

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Project description:BACKGROUND:The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. However, the recent extinction of most Caribbean non-volant mammals has obstructed evolutionary studies, and poor DNA preservation associated with tropical environments means that very few ancient DNA sequences are available for extinct vertebrates known from the region's Holocene subfossil record. The endemic Caribbean eulipotyphlan family Nesophontidae ("island-shrews") became extinct ~?500?years ago, and the taxonomic validity of many Nesophontes species and their wider evolutionary dynamics remain unclear. Here we use both morphometric and palaeogenomic methods to clarify the status and evolutionary history of Nesophontes species from Hispaniola, the second-largest Caribbean island. RESULTS:Principal component analysis of 65 Nesophontes mandibles from late Quaternary fossil sites across Hispaniola identified three non-overlapping morphometric clusters, providing statistical support for the existence of three size-differentiated Hispaniolan Nesophontes species. We were also able to extract and sequence ancient DNA from a?~?750-year-old specimen of Nesophontes zamicrus, the smallest non-volant Caribbean mammal, including a whole-mitochondrial genome and partial nuclear genes. Nesophontes paramicrus (39-47?g) and N. zamicrus (~?10?g) diverged recently during the Middle Pleistocene (mean estimated divergence?=?0.699?Ma), comparable to the youngest species splits in Eulipotyphla and other mammal groups. Pairwise genetic distance values for N. paramicrus and N. zamicrus based on mitochondrial and nuclear genes are low, but fall within the range of comparative pairwise data for extant eulipotyphlan species-pairs. CONCLUSIONS:Our combined morphometric and palaeogenomic analyses provide evidence for multiple co-occurring species and rapid body size evolution in Hispaniolan Nesophontes, in contrast to patterns of genetic and morphometric differentiation seen in Hispaniola's extant non-volant land mammals. Different components of Hispaniola's mammal fauna have therefore exhibited drastically different rates of morphological evolution. Morphological evolution in Nesophontes is also rapid compared to patterns across the Eulipotyphla, and our study provides an important new example of rapid body size change in a small-bodied insular vertebrate lineage. The Caribbean was a hotspot for evolutionary diversification as well as preserving ancient biodiversity, and studying the surviving representatives of its mammal fauna is insufficient to reveal the evolutionary patterns and processes that generated regional diversity.

Project description:The characterization and preservation of genetic variation in crops is critical to meeting the challenges of breeding in the face of changing climates and markets. In recent years, the use of single nucleotide polymorphisms (SNPs) has become routine, allowing us to understand the population structure, find divergent lines for crosses, and illuminate the origin of crops. However, the focus on SNPs overlooks other forms of variation, such as copy number variation (CNVs). Lentil is the third most important cold-season legume and was domesticated in the Fertile Crescent. We genotyped 324 accessions that represent its global diversity, and using both SNPs and CNVs, we dissected the population structure and genetic variation, and identified candidate genes. Eight clusters were detected, most of them located in or near the Fertile Crescent, even though different clusters were present in distinct regions. The cluster from South Asia was particularly differentiated and presented low diversity, contrasting with the clusters from the Mediterranean and the northern temperate. Accessions from North America were mainly assigned to one cluster and were highly diverse, reflecting the efforts of breeding programs to integrate variation. Thirty-three genes were identified as candidates under selection and among their functions were sporopollenin synthesis in pollen, a component of chlorophyll B reductase that partially determines the antenna size, and two genes related to the import system of chloroplasts. Eleven percent of all lentil genes and 21% of lentil disease resistance genes were affected by CNVs. The gene categories overrepresented in these genes were "enzymes," "Cell Wall Organization," and "external stimuli response." All the genes found in the latter were associated with pathogen response. CNVs provided information about population structure and might have played a role in adaptation. The incorporation of CNVs in diversity studies is needed for a broader understanding of how they evolve and contribute to domestication.

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Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation.

Publications

Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation.

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