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Post-Weaning Cranial Growth in Shrew Opossums (Caenolestidae): a Comparison with Bandicoots (Peramelidae) and Carnivorous Marsupials

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Post-Weaning Cranial Growth in Shrew Opossums (Caenolestidae): a Comparison with Bandicoots (Peramelidae) and Carnivorous Marsupials J Mammal Evol DOI 10.1007/s10914-014-9279-0 ORIGINAL PAPER Post-Weaning Cranial Growth in Shrew Opossums (Caenolestidae): A Comparison with Bandicoots (Peramelidae) and Carnivorous Marsupials David A. Flores & Fernando Abdala & Gabriel M. Martin & Norberto P. Giannini & Juan M. Martinez & Grupo Mastozoología # Springer Science+Business Media New York 2014 Abstract The patterns of development and skull ontogeny in optimization of the confidence intervals of the variables ana- caenolestids have been poorly studied, resulting in a limited lyzed in two alternative hypotheses, where Ameridelphia is knowledge. In this work, we report and compare the allome- considered as monophyletic and paraphyletic. Rhyncholestes tric growth trends of 15 variables in the three living groups of raphanurus and C. fuliginosus shared more allometric trends the Family Caenolestidae, represented by Caenolestes than any other between-taxa comparisons. Notwithstanding, fuliginosus, Lestoros inca, and Rhyncholestes raphanurus. several statistics were higher in R. raphanurus, except for We analyzed the bivariate and multivariate allometry in com- those variables related to temporal muscles and bite. The close parison with morphologically convergent Australasian relationship between R. raphanurus and L. inca is also sup- peramelids, as well as with other marsupials and placentals ported by the longitudinal growth of the rostrum, although previously studied. We also report the phylogenetic signal and with a clear growth extension in R. raphanurus. The allome- tric trends reported for L. inca reflect a more predaceous Electronic supplementary material The online version of this article condition compared to other caenolestids. Bandicoots and (doi:10.1007/s10914-014-9279-0) contains supplementary material, caenolestids did not show a particularly shared growth pattern, which is available to authorized users. with the latter being morphologically more conservative. D. A. Flores (*) Ameridelphia was paraphyletic in the shortest tree regarding División Mastozoología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470, CP1405 Buenos the optimization of the confidence intervals. However, the Aires, Argentina growth of several variables supported monophyletic groups e-mail: [email protected] in both hypotheses. Skull ontogeny in marsupials is informa- tive in several aspects of the mandible and neurocranium D. A. Flores : G. M. Martin : N. P. Giannini CONICET, Consejo Nacional de Investigaciones Científicas y reflecting the high phylogenetic signal displayed by variables Técnicas related to these cranial regions. URL: http://www.conicet.gov.ar/ . F. Abdala Keywords Caenolestidae Ontogeny Growth evolution Evolutionary Studies Institute, University of the Witwatersrand, Marsupials Johannesburg, South Africa G. M. Martin Laboratorio de Investigaciones en Evolución y Biodiversidad, Introduction Universidad Nacional de la Patagonia, Esquel, Argentina Extant marsupials exhibit high morphological variation in N. P. Giannini Cátedra de Biogeografía, Facultad de Ciencias Naturales, skull morphology (e.g., Wroe and Milne 2007; Goswami Universidad Nacional de Tucumán, San Miguel de Tucumán, et al. 2011, 2012; Bennett and Goswami 2013). Recent com- Argentina parative studies in marsupials and placentals (e.g., Wilson and Sánchez-Villagra 2010; Wilson 2013) suggest that the former J. M. Martinez Grupo Mastozoología & Colección Teriológica, Universidad de show less disparity in the general morphology of the skull, but Antioquia, Medellín, Colombia higher integration, mostly in the oral region (e.g., Shirai and J Mammal Evol Marroig 2010; Porto et al. 2013). In marsupials, the rostral i1 (Hershkovitz 1995). In turn, bandicoots possess a region is initially constrained by its functional compromise tarsal morphology typical of Australasian marsupials from attachment for suckling during early stages of develop- (Szalay 1982), unpaired spermatozoa (Tyndale-Biscoe ment (Bennett and Goswami 2013). Such differences are 2005), and a chorioallantoic placenta (Hughes et al. probably caused by intrinsic factors (especially the mode of 1990; Tyndale-Biscoe 2005), which is functionally relat- marsupial reproduction and development, Goswami et al. ed to a fast rate of development in this group (Gordon 2012) and/or extrinsic ones (history of diversification and and Hulbert 1989). biogeography, Sánchez-Villagra 2013). However, in spite of In the balance of all evidence, the two long-nosed clades of the lower developmental disparity reported for marsupials in living marsupials appear to be convergent and not closely comparison with placentals, the former group exhibits high related phylogenetically. Caenolestids are the only extant rep- morphological diversity including both specialized (e.g., resentatives of the once diverse order Paucituberculata strictly herbivorous, nectarivorous, or carnivorous groups) as (Abello 2007; Patterson 2008), which includes several spe- well as generalized forms showing morphological conver- cialized forms that had their richness peak during the middle gences on skull shape (see Wroe and Milne 2007 for Tertiary (Abello 2007, 2013), convergent with other carnivores). “pseudodiprotodont” fossils such as Polydolopimorphia The Australasian bandicoots (Peramelidae) and the South (Goin et al. 2003). American shrew opossums (Caenolestidae), exhibit similar Regarding bandicoots, until recently the scarce ontogenetic skull features such as a greatly elongated rostrum and large data published were limited to aging of specimens on the basis palatine vacuities, which distinguish both from other extant of tooth eruption (e.g., Kingsmill 1962; Lyne 1964;Lyneand marsupials. This resemblance between bandicoots and shrew Mort 1981). Recently, Travouillon et al. (2014) described some opossums, which is apparent in spite of well-marked differ- cranial ontogenetic changes in the fossil Madju variae,and ences in body size (e.g., Osgood 1921;Retiefetal.1995; Flores et al. (2013) quantified the pattern of skull growth in Krajewski et al. 1997; Palma and Spotorno 1999), represented Echymipera kalubu and Isoodon macrourus.Thisstudy the basis for old hypotheses of a close relationships between showed that positive allometries apply to longitudinal dimen- both groups (see Osgood 1921;Gregory1922). Several stud- sions in E. kalubu, whereas positive allometries are restricted ies have placed caenolestids in different relationships with to vertical dimensions of the skull in I. macrourus. By contrast, other marsupials (Beck 2008; Meredith et al. 2008). They information on ontogeny is lacking in caenolestids, beyond a have been recovered as the sister group to Didelphimorphia reported slow rate of development for the group (Tyndale- within Ameridelphia (Szalay 1982, 1994; Gemmell and Biscoe 2005), and just a few studies dealing with dental Westerman 1994; Retief et al. 1995; Colgan 1999); sister homologies and tooth replacement / eruption (e.g., Luckett group to the entire Australian marsupial radiation and separate and Hong 2000; Martin 2007, 2013). Breeding data are re- from Ameridelphia (Springer et al. 1998; Amrine-Madsen stricted to anecdotal records (see Patterson and Gallardo 1987). et al. 2003; Horovitz and Sánchez-Villagra 2003;Asher Extant caenolestids represent excellent candidates for com- et al. 2004;Cardilloetal.2004; Nilsson et al. 2004; parative studies of skull growth with convergent Australasian Munemasa et al. 2006; Beck 2008;Becketal,2008); sister forms, the bandicoots, and with other marsupials, given the to both Didelphimorphia and all Australian marsupials wealth of recent studies on the allometry of skull growth in (Kirsch et al. 1991;SzalayandSargis2001); or as the sister marsupials from several groups from both the Australasian group to Peramelemorphia and different from the rest of all and American radiations (e.g., Abdala et al. 2001; Flores et al. marsupials (Palma and Spotorno 1999). Another recent 2003, 2006, 2010, 2013;Gianninietal.2004). Flores et al. phyogeny placed the caenolestids in a position closely related (2013) compared the allometric growth pattern of two bandi- to bandicoots (Lavedèze and Muizon 2010). Despite this coots with previously studied marsupials and placentals (three conflicting phylogenetic information, caenolestids exhibit a didelphids, two australidelphians, two primates, and two plesiomorphic tarsal morphology similar to that of other New carnivorans). The two bandicoots showed ontogenetic trajec- World marsupials (Szalay 1982, 1994), paired spermatozoa as tories that differed in several measurements, suggesting a clear in most New World marsupials, albeit with unique character- divergence in the growth patterns between them. However, istics (Biggers and DeLamater 1965; Temple-Smith 1987), and in agreement with those studies that suggest a low mor- enlarged and forwardly projected first lower incisors phological disparity in the neurocranium of marsupials (e.g., (Marshall 1980; Patterson 2008), large antorbital vacuities Bennett and Goswami 2013), the allometric trends of sensorial (Marshall 1980; Patterson and Gallardo 1987), and a shrew- capsules scaled mostly with negative allometry in all groups like external appearance (Palma 2003).Thepairoflarge, (Flores et al. 2013). The higher degree of integration of forwardly directed incisors in the lower jaw resemble the viscerocranium in marsupials (Bennett and Goswami those of Diprotodontia (Osgood 1924), but they are ap- 2013) is in general agreement
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