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The Evolutionary History of Sigmodontine Rodents in Patagonia and Tierra Del Fuego

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The Evolutionary History of Sigmodontine Rodents in Patagonia and Tierra Del Fuego Biological Journal of the Linnean Society, 2011, 103, 495–513. With 7 figures The evolutionary history of sigmodontine rodents in Patagonia and Tierra del Fuego ULYSES F. J. PARDIÑAS1,*, PABLO TETA2, GUILLERMO D’ELÍA3 and ENRIQUE P. LESSA4 1Centro Nacional Patagónico, CC 128, 9120 Puerto Madryn, Chubut, Argentina 2Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina 3Instituto de Ecología y Evolución, Universidad Austral de Chile, campus Isla Teja s/n, Valdivia, and Centro de Investigación en Ecosistemas de la Patagonia, Coyhaique, Chile 4Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay Received 1 March 2011; accepted for publication 1 March 2011bij_1679 495..513 The Patagonian and Fuegian regions host a rich assemblage of sigmodontine rodents. In this article, we present a synthesis of our current understanding of their late Neogene diversification. Sigmodontine diversity in this area encompasses 16 genera and about 24 species; however, most belong to the tribes Abrotrichini and Phyllotini. Several abrotrichine genera are endemic to the region, whereas phyllotines are represented mainly by species widely distributed outside Patagonia. Two main ecogeographical assemblages of sigmodontines can be recognized: a lowland northeastern group with species mostly associated with shrub formations of the Monte Desert, and a medium to highland southwestern group of typical Patagonian elements, including several abrotrichines and a diversity of Andean forms. The pattern of latitudinal decline in species’ number in sigmodontine rodents is more complex than the traditionally envisioned north to south pauperization; southern mainland Patagonia is as poor in species’ number as is northern Tierra del Fuego (six species), suggesting that insularity is insufficient to explain the island assemblage. Glacial cycles may have had a major role in the control of sigmodontine richness. The fossil Fuego–Patagonian sigmodontine record is restricted to late Pleistocene–Holocene times. Remarkable events include regional extinctions of several widespread southwestern species during the latest Holocene and a reworking of micromammal assemblages, probably as a result of anthropogenic environmental changes. Two main phylogeo- graphical patterns can be broadly associated with the northeastern and southwestern groups. The northeastern assemblage basically comprises species without phylogeographical structure, whereas the southwestern group involves several lineages with deep phylogeographical breaks. The current Fuego–Patagonian sigmodontine assemblage is mainly composed of species that colonized the area from lower latitudes and by others that have differentiated in situ. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 495–513. ADDITIONAL KEYWORDS: Argentina – Cricetidae – extinctions – phylogeography – Quaternary – refugia – Sigmodontinae. La región Patagónico-Fueguina comporta un rico ensamble de roedores sigmodontinos. En este trabajo presentamos una síntesis del conocimiento sobre los procesos de diversificación del grupo durante el Neógeno tardío. La diversidad de sigmodontinos comprende 16 géneros y cerca de 24 especies; sin embargo, la mayor parte de las mismas pertenecen a las tribus Abrotrichini y Phyllotini. Varios géneros de abrotriquinos son endémicos de la región, mientras que los filotinos están en general representados por especies de amplia distribución fuera de Patagonia. Se pueden reconocer dos grandes ensambles eco-geográficos de sigmodontinos: un grupo nor-oriental de tierras bajas, con especies mayoritariamente asociadas a las formaciones vegetales arbustivas del Monte, y otro *Corresponding author. E-mail: [email protected] © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 495–513 495 496 U. F. J. PARDIÑAS ET AL. sud-occidental de tierras de mediana a alta elevación, que agrupa típicos elementos patagónicos, incluyendo abrotriquinos y una diversidad de formas andinas. El patrón de disminución latitudinal en el número de especies de sigmodontinos es más complejo que aquel tradicionalmente supuesto de una pauperización norte a sur. La porción continental más austral de Patagonia es tan pobre en número de especies como la porción norte de Tierra del Fuego (seis especies) sugiriendo que la insularidad es insuficiente para explicar el ensamble isleño. Los ciclos glaciales podrían haber jugado un papel principal en el control de la riqueza específica de sigmodontinos y mamíferos en general. El registro fósil de sigmodontinos en Fuego-Patagonia está restringido al Pleistoceno tardío y Holoceno. Eventos destacables en esta historia incluyen extinciones regionales de especies sud-orientales de amplia distribución durante el Holoceno tardío y una restructuración de las comunidades posiblemente debida a cambios ambientales de origen antrópico reciente. Dos patrones filogeográficos principales pueden ser gruesamente asociados con los grupos nor-oriental y sud-occidental previamente reseñados. Mientras que el ensamble nor-oriental comprende básicamente especies sin estructura filogeográfica, el sud-occidental involucra varios linajes que muestran profundos quiebres. La fauna de sigmodontinos de Fuego-Patagonia está conformada mayoritariamente por especies que colonizaron desde bajas latitudes y por otras diferenciadas in situ. PALABRAS CLAVE: Argentina – Cricetidae – Extinciones – Filogeografía – Cuaternario – Refugios – Sigmodontinae. INTRODUCTION uneven, positively biased towards the northwestern Relative to its surface area and latitudinal placement, forest–steppe ecotone (the area around the city of the Patagonian–Fuegian region supports a high San Carlos de Bariloche); in contrast, the central diversity of land mammals. From the Río Negro Prov- and austral tablelands are particularly under- ince in the north to the Isla Grande de Tierra del represented in the literature (e.g. Pearson & Fuego in the southern tip (Tierra del Fuego, hereaf- Pearson, 1982; Monjeau et al., 1998; Pardiñas et al., ter), about 80 species have been recorded (Table S1, 2003). Most of the taxonomic work on Patagonian see Supporting Information). More than 50% of them field mice was produced between the end of the 19th are rodents, and a single subfamily, the Sigmodon- and the first decade of the 20th centuries (cf. tinae (Cricetidae), is represented by 16 genera and Osgood, 1943). Indeed, many genera that character- about 24 species. Interestingly, sigmodontine diver- ize Patagonia – Chelemys, Euneomys, Loxodontomys, sity is largely restricted to the tribes Abrotrichini and Reithrodon, among others – are in need of system- Phyllotini (two of at least nine tribes of Sigmodon- atic revision. Finally, until very recently, there were tinae), and the former has a substantial part of its no more than a few phylogeographical studies of diversity associated with the region. sigmodontine genera of the region (e.g. Hillyard The variety and abundance of Fuego–Patagonian et al., 1997; Kim et al., 1998). field mice, as well as the poor representation of other During the last decade, several research efforts extra-Patagonian speciose groups, such as marsupials have produced rich data on the systematics and and bats, have long been recognized in the literature biogeography of Fuegian–Patagonian sigmodontine (e.g. Darwin, 1839; Allen, 1905; Osgood, 1943; rodents (e.g. Smith, Kelt & Patton, 2001; Pardiñas Pearson, 1983). The study of Fuego–Patagonian sig- et al., 2008; Rodríguez-Serrano, Hernández & Palma, modontine diversity and evolutionary history has 2008; Teta, Udrizar Sauthier & Pardiñas, 2009; Feijoo increased in intensity in recent years, as documented et al., 2010; Lessa, D’Elía & Pardiñas, 2010; Palma, below. However, there have been few efforts to provide Cancino & Rodríguez-Serrano, 2010). In the present a synthesis of our knowledge of the group in the contribution, we address three main topics: (1) the region. recent diversity and latitudinal pattern of pauperiza- Sigmodontines have a long fossil record in South tion; (2) fossil history; and (3) phylogeographical pat- America, with the oldest remains aged at about terns. Our emphasis is on the Argentine drylands 5 Ma (Prevosti & Pardiñas, 2009). In contrast, the (39–56°S), but we also consider available data on more ancient Patagonian fossils are from late adjacent Valdivian and Magellanic forests. The final Pleistocene deposits (e.g. Pearson, 1987; Pardiñas goal of this review is to provide a baseline for the & Teta, 2008), thus providing a very short time understanding of the evolution and historical bioge- window to explore evolutionary processes. The ography of the sigmodontines in the southern portion knowledge of the Patagonian living assemblages is of South America. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 495–513 SIGMODONTINE RODENTS OF FUEGO–PATAGONIA 497 THE RECENT SIGMODONTINE FAUNA seem to be more strictly related to arid and semi-arid SPECIES’ COMPOSITION environments (Hershkovitz, 1962; Mares, 1980), whereas abrothrichines are also associated with Sigmodontine rodents in Fuego–Patagonia mostly southern Andean forests. comprise members of two tribes: abrotrichines and Euneomys and Reithrodon are two very peculiar phyllotines (Table 1; Fig. 1). sigmodontines that were once considered to be The Abrotrichini, a recently recognized tribe extir- members of the Phyllotini (Steppan, 1995), but have pated
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