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Gross Stomach Morphology in Akodontine Rodents (Cricetidae: Sigmodontinae: Akodontini): a Reappraisal of Its Significance in a Phylogenetic Context

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Gross Stomach Morphology in Akodontine Rodents (Cricetidae: Sigmodontinae: Akodontini): a Reappraisal of Its Significance in a Phylogenetic Context See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/341161965 Gross stomach morphology in akodontine rodents (Cricetidae: Sigmodontinae: Akodontini): a reappraisal of its significance in a phylogenetic context Article in Journal of Mammalogy · May 2020 DOI: 10.1093/jmammal/gyaa023 CITATIONS READS 7 327 7 authors, including: Ulyses Pardiñas Carola Canon Instituto de Diversidad y Evolución Austral, Consejo Nacional de Investigaciones Cie… 18 PUBLICATIONS 127 CITATIONS 350 PUBLICATIONS 5,420 CITATIONS SEE PROFILE SEE PROFILE Jorge Brito M. Nuria Cecilia Bernal Hoverud Instituto Nacional de Biodiversidad (INABIO), Ecuador Wildlife Conservation Society 169 PUBLICATIONS 696 CITATIONS 8 PUBLICATIONS 29 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: ORIGINS AND EVOLUTION OF THE TWO SPECIES OF SEA LIONS ENDEMIC FROM GALAPAGOS ISLANDS (ARCTOCEPHALUS GALAPAGOENSIS AND ZALOPHUS WOLLEBAEKI) RELATED WITH THE OTHER SEA LION SPECIES FROM AMERICA BY MEANS OF MITOGENOMICS View project Taxonomic revision of Akodon serrensis View project All content following this page was uploaded by Jorge Brito M. on 05 May 2020. The user has requested enhancement of the downloaded file. applyparastyle "fig//caption/p[1]" parastyle "FigCapt" applyparastyle "fig" parastyle "Figure" Journal of Mammalogy, XX(X):1–23, 2020 Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 DOI:10.1093/jmammal/gyaa023 Gross stomach morphology in akodontine rodents (Cricetidae: Sigmodontinae: Akodontini): a reappraisal of its significance in a phylogenetic context Ulyses F. J. Pardiñas,*, Carola Cañón, Carlos A. Galliari, Jorge Brito , Nuria Bernal Hoverud, Gisele Lessa, and João Alves de Oliveira Instituto de Diversidad y Evolución Austral (IDEAus-CONICET), Boulevard Brown 2915, 9120 Puerto Madryn, Chubut, Argentina (UFJP, CC) Centro de Estudios Parasitológicos y de Vectores (CEPAVE, CONICET-UNLP), calle 120 entre 61 y 62, 1900 La Plata, Buenos Aires, Argentina (CAG) Instituto Nacional de Biodiversidad (INABIO), Rumipamba 341 y Av. de los Shyris, casilla: 17-07-8976, Quito, Ecuador (JB) Wildlife Conservation Society, Programa Bolivia, Casilla 3-35181, San Miguel, La Paz, Bolivia (NBH) Museu de Zoologia, Departamento de Biologia Animal, Universidade Federal de Viçosa, 36571-000 Viçosa, Minas Gerais, Brasil (GL) Museu Nacional, UFRJ, Quinta da Boa Vista, Rio de Janeiro 20940-040, Brasil (JAO) * Correspondent: [email protected] Akodontini, the second largest tribe within sigmodontine rodents, encompasses several stomach morphologies. This is striking because most sigmodontine groups of comparable taxonomic rank are very conservative in this respect. Based on extensive sampling of newly dissected specimens (213 stomachs representing 36 species), as well as published examples, covering almost all akodontine living genera (15 of 16), we undertook a reappraisal of the gross morphology of this organ. We then mapped this information, together with gallbladder occurrence, in a refined multilocus molecular phylogeny of the tribe. We surveyed three different configurations of stomachs in akodontines, according to the degree of development and location of the glandular epithelium; in addition, two minor variations of one of these types were described. Of the five major clades that integrate Akodontini, four are characterized by a single stomach morphology, while one clade exhibits two morphologies. Mapping stomach type on the phylogeny recovered two configurations for the most recent ancestor of Akodontini. A revised survey of gallbladder evidence also revealed overlooked congruencies. The observed stomach diversity and its arrangement in the phylogeny, along with additional morphological characters and the genetic diversity among the main clades, supports the necessity of changes in the current classification of the tribe. Recognition of subtribes or partitioning of Akodontini into several additional tribes of equal rank could be suitable options. Key words: discoglandular, gallbladder, Scapteromyini, unilocular-hemiglandular Akodontini, la segunda mayor tribu de los roedores sigmodontinos, presenta varias morfologías de estómago. Esto es extraño porque la mayor parte de los grupos comparables de sigmodontinos son muy conservadores en este aspecto. Sobre la base de una extensa muestra de nuevos especímenes diseccionados (213 estómagos representando 36 especies), como así también de ejemplos publicados, abarcando la casi totalidad de los géneros vivientes de akodontinos (15 de 16), efectuamos una re-evaluación de la anatomía gruesa de este órgano. Luego, mapeamos esta información, conjuntamente con la ocurrencia de vesícula biliar, en una filogenia molecular multilocus refinada para la tribu. Detectamos tres configuraciones diferentes de estómagos en akodontinos, de acuerdo con el grado de desarrollo y localización del epitelio glandular; adicionalmente, fueron descriptas dos variantes menores de estos tipos. De los cinco clados principales recobrados en Akodontini, cuatro están caracterizados por una única configuración de morfología del estómago y uno exhibe dos morfologías. Las reconstrucciones de los caracteres asociados al estómago sobre la filogenia concuerdan en recuperar dos © The Author(s) 2020. Published by Oxford University Press on behalf of the American Society of Mammalogists, www.mammalogy.org. 1 2 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/advance-article-abstract/doi/10.1093/jmammal/gyaa023/5829685 by ASM Member Access, [email protected] on 05 May 2020 configuraciones en el ancestro más reciente de Akodontini. Una revisión de la evidencia de la vesícula biliar también reveló congruencias hasta ahora inadvertidas. La diversidad estomacal observada y su disposición en la filogenia junto con otros caracteres morfológicos, más la diversidad genética entre los clados principales, sugieren la necesidad de cambios en la clasificación vigente de la tribu. El reconocimiento de subtribus o la partición de los Akodontini en varias unidades de rango tribal podrían ser opciones adecuadas. Key words: Palabras clave, discoglandular, Scapteromyini, unilocular-hemiglandular, vesícula biliar The gross morphology of the stomach was a substantive ele- histological techniques. We therefore discuss neither aspects ment in the classification of cricetid rodents during the 1960s of gland occurrences and distributions nor histochemical is- and 1970s. Vorontsov’s anatomical research of the digestive sues. Brief included notes about gastric arterial irrigation (inter- system (e.g., Vorontsov 1959, 1962, 1967, 1979, 1982) played preted according to Greene 1935:figure 246) are derived from a crucial role in the conformation of cricetid tribes (Vorontsov blood vessels that remained attached to the ectal surface of the 1959). However, despite extensive work by Carleton (1973, stomach, mainly when organs were examined in fresh speci- 1980, 1981), the relevance of the studies of stomach mor- mens. All studied materials (213 stomachs representing 36 spe- phology progressively fell by the wayside. Although data on cies) are listed in Appendix. For those taxa we could not directly gross stomach morphology frequently are included in phylo- study (i.e., Juscelinomys, Kunsia, and Podoxymys), published genetic analyses (e.g., Steppan 1995; Weksler 2006; Pardiñas descriptions were followed (Carleton 1973; Bezerra et al. 2007; et al. 2015d), there is as yet no clear understanding about the and Emmons and Patton 2012, respectively), emended in some significance of its role, if any, in classificatory frameworks. instances through a reinterpretation of stomach anatomy based With respect to the cricetid subfamily Sigmodontinae, most of on the originally provided figures. the currently recognized 11 tribes contained therein are typified Anatomical terms employed in the present contribution are by a singular stomach morphology (Vorontsov 1967; Carleton those defined by Carleton (1973, 1980, 1981), with minor add- 1973). Oryzomyini and Phyllotini, for example, two of the lar- itions according to Vorontsov (1967, 1979), Musser and Durden gest tribal assemblages, exhibit a single-chambered organ where (2002), and Langer (1985, 2017). Carleton (1973:10) recognized glandular and cornified epithelia are distributed more or less two main stomach configurations: unilocular-hemiglandular subequally (Carleton 1973; Weksler 2006). Even minor tribes stomachs (single-chambered organs with a shallow incisura (in number of genera) such as Abrotrichini, Andinomyini, and angularis), and bilocular-discoglandular stomachs, in which Euneomyini, despite trenchant differences among their mem- the main cavity is partially divided by a deep incisura angularis bers in many respects, are conservative in stomach morphology “...imparting a more strongly-defined bipartite condition,” and (Pardiñas et al. 2015d; Salazar-Bravo et al. 2016; Teta et al. 2017). in which the glandular epithelium is restricted to the fundus However, akodontines encompass at least three main types of of the stomach or confined into a pouch (= diverticulum in stomach design judged on the basis of the extension and location Vorontsov 1967:figure 100; = glandular pouch in Musser and of the glandular epithelium (Vorontsov 1967; Carleton 1973). Durden 2002:figure 22). Although Carleton
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