Bats (Chiroptera: Noctilionoidea) Challenge a Recent Origin of Extant Neotropical Diversity
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Syst. Biol. 65(3):432–448, 2016 © The Author(s) 2016. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] DOI:10.1093/sysbio/syw011 Advance Access publication February 10, 2016 Bats (Chiroptera: Noctilionoidea) Challenge a Recent Origin of Extant Neotropical Diversity , ,∗ , , DANNY ROJAS1 2 ,OMAR M. WARSI2 3, AND LILIANA M. DÁVA LO S 2 4 1Department of Biology and Centre for Environmental and Marine Studies, University of Aveiro, 3810-193 Aveiro, Portugal; 2Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building Stony Brook, NY 11794, USA; 3Uppsala Biomedicinskt Centrum BMC, Husarg, 3 751 23 Uppsala, Sweden; 4Consortium for Inter-Disciplinary Environmental Research, School of Marine and Atmospheric Sciences, Stony Brook University, 129 Dana Hall, Stony Brook, NY 11794, USA. ∗ Correspondence to be sent to: Department of Biology and Centre for Environmental and Marine Studies, University of Aveiro, 3810-193 Aveiro, Portugal; E-mail: [email protected] Received 22 August 2014; reviews returned 28 January 2016; accepted 1 February 2016 Associate Editor: Robb Brumfield Abstract.—The mechanisms underlying the high extant biodiversity in the Neotropics have been controversial since the 19th century. Support for the influence of period-specific changes on diversification often rests on detecting more speciation Downloaded from events during a particular period. The timing of speciation events may reflect the influence of incomplete taxon sampling, protracted speciation, and null processes of lineage accumulation. Here we assess the influence of these factors on the timing of speciation with new multilocus data for New World noctilionoid bats (Chiroptera: Noctilionoidea). Biogeographic analyses revealed the importance of the Neotropics in noctilionoid diversification, and the critical role of dispersal. We detected no shift in speciation rate associated with the Quaternary or pre-Quaternary periods, and instead found an increase in speciation linked to the evolution of the subfamily Stenodermatinae (∼18 Ma). Simulations modeling constant speciation and extinction rates for the phylogeny systematically showed more speciation events in the Quaternary. Since recording http://sysbio.oxfordjournals.org/ more divergence events in the Quaternary can result from lineage accumulation, the age of extant sister species cannot be interpreted as supporting higher speciation rates during this period. Instead, analyzing the factors that influence speciation requires modeling lineage-specific traits and environmental, spatial, and ecological drivers of speciation. [Fossils; geographic range evolution; Neotropics; Phyllostomidae; speciation.] The Neotropics harbors the most diverse terrestrial were interpreted as supporting the Quaternary origin ecosystems on Earth, and the mechanisms behind of species diversity in that neotropical clade (Garzón- this high biodiversity have remained contentious Orduña et al. 2014). In contrast, an earlier meta-analysis since the 19th century (Wallace 1853; Bates 1863). of crown group ages from 105 neotropical time- by Liliana Davalos on April 29, 2016 Quaternary climate change (last 2.58 myr) has been calibrated phylogenies found that cladogenesis unfolded invoked for several decades to explain how populations more or less continuously in the Neotropics (Rull 2008), in lowland New World forests became genetically and neither the Quaternary nor the preceding periods isolated, generating many descendant species (Haffer were overwhelmingly more important in speciation 1969; Hooghiemstra and van der Hammen 1998). (see also Zink et al. 2004). Another meta-analysis using Geomorphological (Mayle 2004), paleoecological (Porto crown ages of different clades from northern South et al. 2013), and biogeographic data (Poelchau and America concluded that most extant lineages in the Hamrick 2013), however, suggest other mechanisms region have a pre-Quaternary origin (Hoorn et al. 2010). explain speciation in the region. Vicariance events Even as the debate on the influence on speciation of resulting from the tectonic activity and habitat change geological events during particular periods has been during the pre-Quaternary (mainly the Neogene, reignited, it has become clear that incomplete taxon between 2.58 Ma and 23.03 Ma) have been proposed sampling, protracted speciation (Etienne and Rosindell as an alternative mechanism to explain neotropical 2012), and null processes of lineage accumulation biodiversity (Bush 1994; Hoorn et al. 2010). The strongly influence divergence dates. Crown age and Quaternary and pre-Quaternary hypotheses have been species divergences will also reflect those processes, in treated as mutually exclusive, despite a variety of other addition to any shifts in speciation rates. Testing the possible explanations (e.g., the gradient hypothesis, effects of environmental, spatial, and ecological drivers the riverine barrier hypothesis, or the disturbance– of clade diversity then requires explicit modeling of vicariance hypothesis; see references in Rull 2015). As speciation rates (Rabosky 2014). a result, although a multiple-hypothesis approach has Noctilionoid bats (superfamily Noctilionoidea), and been recommended to study the origin of neotropical in particular fruit-feeding phyllostomids, are among diversity (Rull 2015), most of the debate has focused on the most common and diverse lowland mammals in the the evidence supporting either temporal model. Neotropics (Fleming and Kress 2013). The New World The age of crown groups and divergence times noctilionoid families Thyropteridae, Furipteridae, between sister species are the main evidence used to Noctilionidae, Mormoopidae, and Phyllostomidae support these temporal models, and have been used as account for ∼20% of global species richness among bats proxies for speciation rates during the Neogene or the (Teeling et al. 2005). The past and current distributions Quaternary. For example, analyses of divergence time of two other noctilionoid families—Myzopodidae from for 131 pairs of sister species of neotropical butterflies Madagascar, with fossils in Africa, and Mystacinidae 432 2016 ROJAS ET AL.—DIVERSIFICATION OF NEOTROPICAL BATS 433 from New Zealand, with fossils in Australia—suggest a the inadequacy of divergence times in determining the Gondwanan origin for the superfamily and open new role of climate and habitat change at particular periods questions on when and how ancestral noctilionoids on the speciation process. reached the Americas (Gunnell et al. 2014). Many species of extant New World noctilionoids occur in northern South America (Supplementary Fig. S1; available on MATERIALS AND METHODS Dryad at http://dx.doi.org/10.5061/dryad.s533p), and Taxonomic and Molecular Sampling biogeographic studies in a few genera of phyllostomids have found a South American origin for most species, Generic and species-level taxonomy for followed by dispersals to Central America and the Noctilionoidea follows Simmons (2005), updated Caribbean (Velazco and Patterson 2008, 2013). This following the recent taxonomic literature (Hurtado suggests South America has been an important area for and Pacheco 2014; Parlos et al. 2014; Tavares et al. 2014; diversification of New World noctilionoids, if not their Velazco and Patterson 2014). Subfamily and generic area of origin. These characteristics make noctilionoids taxonomy within Phyllostomidae follows Baker et al. a good study system to analyze the timing of neotropical (2003). We sampled 90% of the 70 genera and 76% of taxonomic diversification. the 254 species described hitherto for the New World Downloaded from Despite their mostly neotropical distribution, there are Noctilionoidea (Supplementary Table S1). The sample fossil and extant noctilionoids outside the Neotropics included the 11 subfamilies of Phyllostomidae and all that suggest a long history in other areas and make neotropical families of the superfamily Noctilionoidea. it critical to estimate their biogeographic history. Early In addition, we used the Old World noctilionoids Oligocene fossils (30.8–33.3 Ma) trace the most ancient Mystacina tuberculata and Myzopoda aurita as outgroups. http://sysbio.oxfordjournals.org/ noctilionoid lineages to North America (Czaplewski This data set included sequences from one undescribed and Morgan 2012; Morgan and Czaplewski 2012). These species of the genus Micronycteris (Porter et al. 2007), records suggest an ancient North American distribution two newly described species, and one undescribed for the two most species-rich noctilionoid families: species in the genus Sturnira (Velazco and Patterson Mormoopidae and Phyllostomidae (Baker et al. 2012; 2014), as well as lineages from populations previously Arita et al. 2014). To date, however, formal biogeographic assigned to Lophostoma silvicolum and Pteronotus parnellii analyses have not been conducted and the mode and rubiginosus that likely represent independently evolving timing of events leading to the present overwhelmingly populations (Porter et al. 2003; Clare et al. 2013). neotropical distributions of noctilionoids remain to be We generated sequences for seven nuclear loci analyzed. (Supplementary Table S2; 661 sequences, 141 taxa): by Liliana Davalos on April 29, 2016 Despite much recent progress, phylogenetic introns of thyrotropin beta chain (thy) and signal relationships within the superfamily remain unclear, in transducer