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Ancient DNA Suggests Single Colonization and Within-Archipelago Diversification of Caribbean Caviomorph Rodents.

ABSTRACT: Reconstructing the evolutionary history of island biotas is complicated by unusual morphological evolution in insular environments. However, past human-caused extinctions limit the use of molecular analyses to determine origins and affinities of enigmatic island taxa. The Caribbean formerly contained a morphologically diverse assemblage of caviomorph rodents (33 species in 19 genera), ranging from ∼0.1 to 200 kg and traditionally classified into three higher-order taxa (Capromyidae/Capromyinae, Heteropsomyinae, and Heptaxodontidae). Few species survive today, and the evolutionary affinities of living and extinct Caribbean caviomorphs to each other and to mainland taxa are unclear: Are they monophyletic, polyphyletic, or paraphyletic? We use ancient DNA techniques to present the first genetic data for extinct heteropsomyines and heptaxodontids, as well as for several extinct capromyids, and demonstrate through analysis of mitogenomic and nuclear data sets that all sampled Caribbean caviomorphs represent a well-supported monophyletic group. The remarkable morphological and ecological variation observed across living and extinct caviomorphs from Cuba, Hispaniola, Jamaica, Puerto Rico, and other islands was generated through within-archipelago evolutionary radiation following a single Early Miocene overwater colonization. This evolutionary pattern contrasts with the origination of diversity in many other Caribbean groups. All living and extinct Caribbean caviomorphs comprise a single biologically remarkable subfamily (Capromyinae) within the morphologically conservative living Neotropical family Echimyidae. Caribbean caviomorphs represent an important new example of insular mammalian adaptive radiation, where taxa retaining "ancestral-type" characteristics coexisted alongside taxa occupying novel island niches. Diversification was associated with the greatest insular body mass increase recorded in rodents and possibly the greatest for any mammal lineage.

SUBMITTER: Woods R

PROVIDER: S-EPMC7783164 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCaviomorph rodents, some of the oldest Leishmania spp. hosts, are widely dispersed in Brazil. Despite both experimental and field studies having suggested that these rodents are potential reservoirs of Leishmania parasites, not more than 88 specimens were analyzed in the few studies of natural infection. Our hypothesis was that caviomorph rodents are inserted in the transmission cycles of Leishmania in different regions, more so than is currently recognized.MethodologyWe investigated the Leishmania infection in spleen fragments of 373 caviomorph rodents from 20 different species collected in five Brazilian biomes in a period of 13 years. PCR reactions targeting kDNA of Leishmania sp. were used to diagnose infection, while Leishmania species identification was performed by DNA sequencing of the amplified products obtained in the HSP70 (234) targeting. Serology by IFAT was performed on the available serum of these rodents.Principal findingsIn 13 caviomorph rodents, DNA sequencing analyses allowed the identification of 4 species of the subgenus L. (Viannia): L. shawi, L. guyanensis, L. naiffi, and L. braziliensis; and 1 species of the subgenus L. (Leishmania): L. infantum. These include the description of parasite species in areas not previously included in their known distribution: L. shawi in Thrichomys inermis from Northeastern Brazil and L. naiffi in T. fosteri from Western Brazil. From the four other positive rodents, two were positive for HSP70 (234) targeting but did not generate sequences that enabled the species identification, and another two were positive only in kDNA targeting.Conclusions/significanceThe infection rate demonstrated by the serology (51.3%) points out that the natural Leishmania infection in caviomorph rodents is much higher than that observed in the molecular diagnosis (4.6%), highlighting that, in terms of the host species responsible for maintaining Leishmania species in the wild, our current knowledge represents only the "tip of the iceberg."

Project description:Vertebrate musculoskeletal locomotion is realized through lever-arm systems. The instantaneous muscle moment arm (IMMA), which is expected to be under selective pressure and thus of interest for ecomorphological studies, is a key aspect of these systems. The IMMA changes with joint motion. It's length change is technically difficult to acquire and has not been compared in a larger phylogenetic ecomorphological framework, yet. Usually, proxies such as osteological in-levers are used instead. We used 18 species of the ecologically diverse clade of caviomorph rodents to test whether its diversity is reflected in the IMMA of the hip extensor M. gluteus medius. A large IMMA is beneficial for torque generation; a small IMMA facilitates fast joint excursion. We expected large IMMAs in scansorial species, small IMMAs in fossorial species, and somewhat intermediate IMMAs in cursorial species, depending on the relative importance of acceleration and joint angular velocity. We modeled the IMMA over the entire range of possible hip extensions and applied macroevolutionary model comparison to selected joint poses. We also obtained the osteological in-lever of the M. gluteus medius to compare it to the IMMA. At little hip extension, the IMMA was largest on average in scansorial species, while the other two lifestyles were similar. We interpret this as an emphasized need for increased hip joint torque when climbing on inclines, especially in a crouched posture. Cursorial species might benefit from fast joint excursion, but their similarity with the fossorial species is difficult to interpret and could hint at ecological similarities. At larger extension angles, cursorial species displayed the second-largest IMMAs after scansorial species. The larger IMMA optimum results in powerful hip extension which coincides with forward acceleration at late stance beneficial for climbing, jumping, and escaping predators. This might be less relevant for a fossorial lifestyle. The results of the in-lever only matched the IMMA results of larger hip extension angles, suggesting that the modeling of the IMMA provides more nuanced insights into adaptations of musculoskeletal lever-arm systems than this osteological proxy.

Project description:The combination of morphometrics, phylogenetic comparative methods, and open data sets has renewed interest in relating morphology to adaptation and ecological opportunities. Focusing on the Caviomorpha, a well-studied mammalian group, we evaluated patterns in research and data sharing in studies relating form and function. Caviomorpha encompasses a radiation of rodents that is diverse both taxonomically and ecologically. We reviewed 41 publications investigating ecomorphology in this group. We recorded the type of data used in each study and whether these data were made available, and we re-digitized all provided data. We tracked two major lines of information: collections material examined and trait data for morphological and ecological traits. Collectively, the studies considered 63% of extant caviomorph species; all extant families and genera were represented. We found that species-level trait data rarely were provided. Specimen-level data were even less common. Morphological and ecological data were too heterogeneous and sparse to aggregate into a single data set, so we created relational tables with the data. Additionally, we concatenated all specimen lists into a single data set and standardized all relevant data for phylogenetic hypotheses and gene sequence accessions to facilitate future morphometric and phylogenetic comparative research. This work highlights the importance and ongoing use of scientific collections, and it allows for the integration of specimen information with species trait data. Recientemente ha resurgido el interés por estudiar la relación entre morfología, ecología, y adaptación. Esto se debe al desarrollo de nuevas herramientas morfométricas y filogenéticas, y al acceso a grandes bases de datos para estudios comparados. Revisamos 41 publicaciones sobre ecomorfología de roedores caviomorfos, un grupo diverso y bien estudiado, para evaluar los patrones de investigación y la transparencia para la liberación de datos. Registramos los tipos de datos que se utilizaron para cada estudio y si los datos están disponibles. Cuando estos datos se compartieron, los redigitalizamos. Nos enfocamos en los ejemplares consultados, y en datos que describen rasgos ecológicos y morfológicos para las especies estudiadas. Los estudios que revisamos abarcan el 63% de las especies de caviomorfos que actualmente existen. Encontramos que raramente fueron compartidos los datos que se tomaron para especies, y menos aún para ejemplares. Los datos morfológicos y ecológicos eran demasiado heterogéneos e exiguos para consolidar en un solo banco de datos; debido a esta circunstancia, creamos tablas relacionales con los datos. Además, enlazamos todas las listas individuales de especímenes para crear un solo banco de datos y estandarizamos todos los datos pertinentes a hipótesis filogenéticas, así como los números de acceso de secuencias genéticas, para así facilitar eventuales estudios comparados de morfometría y filogenia. Este trabajo resalta la importancia de las colecciones científicas y documenta su uso, además permitiendo la futura integración de datos derivados de ejemplares con datos sobre rasgos ecomorfológicos a nivel de especie.

Project description:BackgroundIsland systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investigating evolutionary patterns and processes shaping biotic diversification have focused on more recent (emergent) rather than ancient oceanic archipelagos. Here, we focus on the granitic islands of the Seychelles, which are unusual among island systems because they have been isolated for a long time and are home to a monophyletic radiation of caecilian amphibians that has been separated from its extant sister lineage for ca. 65-62 Ma. We selected the most widespread Seychelles caecilian species, Hypogeophis rostratus, to investigate intraspecific morphological and genetic (mitochondrial and nuclear) variation across the archipelago (782 samples from nine islands) to identify patterns and test processes that shaped their evolutionary history within the Seychelles.ResultsOverall a signal of strong geographic structuring with distinct northern- and southern-island clusters were identified across all datasets. We suggest that these distinct groups have been isolated for ca. 1.26 Ma years without subsequent migration between them. Populations from the somewhat geographically isolated island of Frégate showed contrasting relationships to other islands based on genetic and morphological data, clustering alternatively with northern-island (genetic) and southern-island (morphological) populations.ConclusionsAlthough variation in H. rostratus across the Seychelles is explained more by isolation-by-distance than by adaptation, the genetic-morphological incongruence for affinities of Frégate H. rostratus might be caused by local adaptation over-riding the signal from their vicariant history. Our findings highlight the need of integrative approaches to investigate fine-scale geographic structuring to uncover underlying diversity and to better understand evolutionary processes on ancient, continental islands.

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Ancient DNA Suggests Single Colonization and Within-Archipelago Diversification of Caribbean Caviomorph Rodents.

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