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Influence of Evolutionary Allometry on Rates of Morphological Evolution and Disparity in Strictly Subterranean Moles (Talpinae, Talpidae, Lipotyphla, Mammalia)

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Influence of Evolutionary Allometry on Rates of Morphological Evolution and Disparity in Strictly Subterranean Moles (Talpinae, Talpidae, Lipotyphla, Mammalia) J Mammal Evol DOI 10.1007/s10914-016-9370-9 ORIGINAL PAPER Influence of Evolutionary Allometry on Rates of Morphological Evolution and Disparity in strictly Subterranean Moles (Talpinae, Talpidae, Lipotyphla, Mammalia) G. Sansalone1,2,3 & P. Colangelo 2,4 & T. Kotsakis1,2 & A. Loy2,5 & R. Castiglia6 & A. A. Bannikova7 & E. D. Zemlemerova7 & P. Piras8,9 # Springer Science+Business Media New York 2017 Abstract The adaptation to a particular function could di- size variables. Evolutionary allometric trajectories exhibited rectly influence the morphological evolution of an anatomi- convergence of humeral shape between the two tribes, even cal structure as well as its rates. The humeral morphology of when controlling for phylogeny, though a significant differ- moles (subfamily Talpinae) is highly modified in response to ences in the evolutionary rates was found between the two intense burrowing and fully fossorial lifestyle. However, lit- tribes. Talpini, unlike Scalopini, seem to have reached a tle is known of the evolutionary pathways that marked its robust fossorial morphology early during their evolution, diversification in the two highly fossorial moles tribes and their shape disparity did not change, if it did not de- Talpini and Scalopini. We used two-dimensional landmark- crease, through time. Furthermore, the basal Geotrypus spp. based geometric morphometrics and comparative methods to clearly set apart from the other highly fossorial moles, understand which factors influenced the rates and patterns of exhibiting a significant acceleration of evolutionary shifts the morphological evolution of the humerus in 53 extant and toward higher degree of fossorial adaptation. Our observa- extinct species of the Talpini (22 extant plus 12 extinct) and tions support the hypothesis that the evolution of allometry Scalopini(sixextantplus13extinct)tribes,foratotalof623 may reflect a biological demand (in this case functional) that humeri. We first built a synthetic phylogeny of extinct and constrains the rates of evolution of anatomical structures. extant taxa of the subfamily Talpinae based on all the avail- able information from known phylogenies, molecular data, and age ranges of fossil records. We tested for evolutionary Keywords Talpinae . Humerus . Evolutionary allometry . allometry by means of multivariate regression of shape on Geometric morphometrics . Comparative methods Electronic supplementary material The online version of this article (doi:10.1007/s10914-016-9370-9) contains supplementary material, which is available to authorized users. * G. Sansalone 5 Environmetrics Lab, Dipartimento STAT, Università del Molise, [email protected] I-86090 Pesche, Italy 6 Department of Biology and Biotechnology BCharles Darwin^, 1 Department of Sciences, Roma Tre University, Largo San Leonardo BSapienza^, University of Rome, Via Borelli 50, I-00161 Rome, Italy Murialdo 1, I-00146 Rome, Italy 7 Lomonosov Moscow State University, Vorobyevy Gory, 2 Center for Evolutionary Ecology, Largo San Leonardo Murialdo 1, Moscow 119992, Russia I-00146 Rome, Italy 8 3 Dipartimento di Scienze Cardiovascolari,Respiratorie, Nefrologiche, Form, Evolution and Anatomy Research Laboratory, Zoology, B ^ School of Environmental and Rural Sciences, University of New Anestesiologiche e Geriatriche, Sapienza , Rome, Italy England, Armidale, NSW 2351, Australia 9 Dipartimento di Ingegneria Strutturale e Geotecnica, Sapienza, 4 National Research Council, Institute of Ecosystem Study, Largo Università di Roma, Via Eudossiana 18, 00100, Rome, Italy Tonolli 50, 28922 Verbania Pallanza (VB), Italy Università di Roma, Via del Policlinico 155, 00161 Rome, Italy J Mammal Evol Introduction Piras et al. (2012) combined geometric morphometrics and phylogenetic comparative methods to study the humeral bio- The heterogeneous dynamics of morphological evolution mechanical performance and morphology in 30 genera of both have been recently emphasized by different authors extant and extinct talpids. According to their results, the rate of (Hopkins and Smith 2015; Slater 2015), who showed that the phenotypic evolution of the highly fossorial species’ hu- different evolutionary processes could influence evolutionary meri underwent a drastic reduction when compared with the rates and morphological disparity through time. Furthermore, rate of other talpid clades not adapted to an underground life- these same authors highlighted that, although the peak of mor- style. Furthermore, Piras et al. (2012, 2015)showedthathigh- phological diversification might occur at any time along a ly fossorial moles reached a functional optimum early in their clade history, the possibility of detecting these changes strong- evolution and then did not experience further significant ly depends on the temporal and taxonomic scale of observa- changes. Their results appear to be congruent with an early tion (Hopkins and Smith 2015;Slater2015). burst mode of evolution and niche filling (Freckleton and Assessing how rates of morphological evolution change Harvey 2006; Slater et al. 2010). However, as reported by through time is challenging. In recent years, many different Slater (2015), early rapid morphological evolution is rare methods have been proposed (O’Meara et al. 2006; Eastman (Harmon et al. 2010). In this framework, we present a new et al. 2011;Beaulieuetal.2012; Thomas and Freckleton study on the rates of phenotypic evolution of humeri in talpids, 2012; Ingram and Mahler 2013; among others) to detect the focusing solely on highly fossorial moles to understand if the rate bursts within a clade’s phylogenetic history. Some of evolution of fossoriality followed different evolutionary path- these methods can handle multivariate data by fitting multiple ways within and/or between the two tribes, Scalopini and Ornstein Uhlenbeck (OU) optima on a tree (Thomas and Talpini. The humerus of moles is particularly interesting be- Freckleton 2012; Ingram and Mahler 2013).Thesearchfor cause it is the bone of the forearm that experienced the most the mechanisms underlying the evolution of a particular ana- remarkable transformations (Dobson 1883; Freeman 1886; tomical structure in a clade could be directly influenced by Edwards 1937; Campbell 1939; Reed 1951; Yalden 1966; that structure’s adaptive function. Gambaryan et al. 2003; Sánchez-Villagra et al. 2004). This The subfamily Talpinae includes the most specialized bone is widened and flattened in response to intense species for burrowing within Talpidae (Yates and Moore burrowing. It has an elliptically shaped (ventrally directed) 1990), representing a paradigmatic group for the study of head, a heavily-expanded proximal end, an enlarged teres tu- phenotypic evolutionary rates under highly selective con- bercle, a deep brachialis fossa, a large, hemicylindrical clavic- straints (i.e., an underground lifestyle; Nevo 1979). The sub- ular facet, and an enlarged medial epicondyle bearing a deep family includes two tribes: the Talpini and the Scalopini fossa for the attachment of the flexor digitorum profundus (Hutterer 2005). The genus Geotrypus (which includes nine tendon-muscle (Hutchison 1968; Gambaryan et al. 2003). species), basal to Talpini, exhibits several primitive morpho- The complexity of humeral modifications makes this bone a logical characters linked to the highly fossorial status and, in potentially rich source of evolutionary informative characters the context of their tribe, represents a distinctive morpholog- (Sánchez-Villagra et al. 2004). Moreover, this bone experi- ical and phylogenetic group (Schwermann and Thompson enced transformations that are of taxonomic and systematic 2015). The fossil record of Talpinae is well documented, relevance, and is further considered to be a good proxy for a with several extinct species described in the literature mole’s body size (Skoczen 1993; van den Hoek Ostende, (Ziegler 1999; Gunnell et al. 2008), and it is largely accept- 1997; Ziegler 2003, 2006; Klietmann et al. 2014;Sansalone ed that the North American (Scalopini) and Eurasian et al. 2015, 2016). The humeral morphology of Talpinae is (Talpini) highly fossorial moles are sister clades (Shinohara highly modified and adapted for complex tunnel digging in et al. 2003;Cabriaetal.2006; Sánchez-Villagra et al. 2006; both Talpini and Scalopini, but the morphological differences Crumpton and Thompson 2013;Schwermannand exhibited in these two tribes are primarily related to the teres Thompson 2015). However, there are still some uncertainties tubercle, the bicipital tunnel, and the pectoral ridge (Sánchez- about the moles’ origin (Hutchison 1974; Sánchez-Villagra Villagra et al. 2006). Despite the abundant literature about the et al. 2006; Schwermann and Thompson 2015). Provided functional morphology of the talpid forelimb (Gambaryan with evidence that the oldest representative of this clade et al. 2003; Scott and Richardson 2005 ; Piras et al. 2012, comes from the early Oligocene of Germany, it was hypoth- 2015), there are no contributions aimed at directly testing the esized that the subfamily originated in Eurasia (Ziegler phylogenetic trajectories of the humeral morphology exclu- 2012). During the Neogene, the Talpinae spread across the sively within highly fossorial moles. Palearctic (Ziegler 1999 ; Gunnell et al. 2008), although it is In the present paper we provide, for the first time, a com- not clear how many invasions occurred through North prehensive set of analyses directly aimed at investigating, by America, across which route (s), or if there
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