Genetic and ecological processes promoting early diversification in the lowland Mesoamerican bat Sturnira parvidens (Chiroptera: Phyllostomidae)

https://doi.org/10.1016/j.ympev.2017.06.015Get rights and content

Highlights

  • Historical and ecological events have shaped the evolutionary history of S. parvidens.

  • Some of the most intense Pleistocene oscillations are involved on its evolution.

  • Differentiation in environmental space prevents admixture of genetic lineages.

Abstract

With 22 species, Sturnira is the most speciose genus of frugivorous Neotropical bats. Sturnira parvidens inhabits lowland tropical areas from Mexico to Central America. The elevation of this taxon to species level was recent, and discrepancies with respect to its geographic limits and phylogenetic position continue to exist. In order to identify genetic and ecological processes likely involved in the diversification and current distribution of S. parvidens, we evaluated relationships, researched phylogeographic and demographic history, and tested the divergence/conservatism of the climatic niche of this bat. We used data from mitochondrial loci (cytochrome b and the hypervariable D-loop region I) and the nuclear recombination activating gene 1, in 173 samples of S. parvidens and 77 samples of related species. We performed Bayesian analyses to infer phylogenetic relationships and analyzed phylogeographic structure, genetic diversity, divergence times and historical demography. Sturnira bakeri is the sister group of S. parvidens, and inhabits Western Ecuador. The two species diverged c. 1.84 Ma, and their distributions are disjunct and separated by Sturnira luisi. Within S. parvidens there are two haplogroups with nearly allopatric distributions that are limited to the Sierra Madre del Sur, on the Mexican Pacific Slope. The divergence time between haplogroups was c. 0.423 Ma and we detected signals of demographic expansion. We also analyzed 526 occurrence data of S. parvidens to test for changes in environmental niche of this species. We detected signals of divergence of climatic niche, mainly in temperature and seasonality variables. Likely, both genetic and ecological processes have shaped the evolutionary history of S. parvidens. Despite many climatic fluctuations during the Pleistocene, only the most intense oscillations had an impact on these bats. In addition, ecological differentiation prevents admixture of genetic lineages that are in contact and lack apparent geographical barriers at the southern Sierra Madre del Sur. We concluded that speciation in Sturnira was promoted by this taxon’s ability to colonize new geographical and environmental spaces and form genetically structured groups when populations become isolated.

Introduction

Geographic position, complex tectonic and orogenic history, climate patterns, and abrupt topography have acted together to generate high biodiversity in Mesoamerica (Bryson et al., 2011). This transitional area between biota from North and South America includes the Neotropical region from Mexico to Central America, and it has been considered one of the most intricate, complex, and diverse areas in the world (León-Paniagua et al., 2007, Myers et al., 2000). In addition to orogenic processes during the Miocene, two major biogeographic events are recognized as generators of biodiversity: the emergence of the Isthmus of Panama, which allowed species flow between previously isolated continents, and climatic oscillations during the Pleistocene, which modified climate, vegetation, and sea levels on a global scale (Gutiérrez-García and Vázquez-Domínguez, 2013).

Although the geographic position of Mesoamerica caused the effect of these climate changes to be less drastic than in areas near the poles, the biological consequences were heterogeneous and complex because its intricate topography affected climatic patterns both latitudinally and altitudinally (Moreno-Letelier and Piñero, 2009). One way to investigate the evolutionary processes that species experienced during this period of time is through phylogeographic studies. This discipline focuses on the recent history of species by analyzing the geographical and temporal variation of intra-specific lineages or of closely related species (Avise, 2000). While recent research has considered Mesoamerica, most of these works have focused on montane regions (e.g., Ornelas et al., 2013, Ramírez-Barahona and Eguiarte, 2013). Although there are some reports of genetic structure and early diversification processes in various lowland taxa, such as reptiles (Suárez-Atilano et al., 2014), birds (Arbeláez-Cortés et al., 2014), and mammals (Arteaga et al., 2012), there are few studies in Mesoamerican lowlands.

In addition to historical events, ecological processes also influence the distribution of genetic variation among populations (Gutiérrez-Rodríguez et al., 2011), and are key in most speciation scenarios (Avise, 2000). For example, significant environmental niche differentiation occurs in association with most speciation events (Warren et al., 2008). Studies that combine phylogeographical and ecological niche analyses are essential to better understand the factors implicated in population differentiation (Rodríguez-Gómez et al., 2013). These analyses are critical for understanding how ecological factors are linked to species formation, and are also useful in the detection of cryptic lineages in widespread morphologically conserved taxa, and for identifying species boundaries at early stages of speciation (Wiens, 2004a).

One genus of bats that contains morphologically conserved species is Sturnira (Chiroptera: Phyllostomidae). It is the most speciose genus of frugivorous Neotropical bats, comprising 22 species (Molinari et al., 2017, Velazco and Patterson, 2013) and includes three early-diverging Andean species (S. aratathomasi, S. bidens, and S. nana), a clade formed by 12 species that are usually found in montane forests (S. adrianae, S. bogotensis, S. burtonlimi, S. erythromos, S. hondurensis, S. koopmanhilli, S. ludovici, S. magna, S. mordax, S. oporaphilum, S. perla, and S. tildae; hereafter clade A), and seven species that inhabit lowland tropical forest and Caribbean islands (S. angeli, S. bakeri, S. lilium, S. luisi, S. new species 3, S. paulsoni, and S. parvidens; hereafter clade B). Sturnira parvidens inhabits Mesoamerican lowlands.

When initially described, S. parvidens was considered a subspecies of S. lilium. Nevertheless, molecular reviews of the Sturnira genus suggested that these two taxa deserved recognition as distinct species (Iudica, 2000, Velazco and Patterson, 2013). However, there is no consensus on inter-specific relationships within the clade of lowland Sturnira (Clare et al., 2011, Ditchfield, 2000, Hajibabaei et al., 2007, Iudica, 2000, Velazco and Patterson, 2013). There is also no consensus concerning the southern geographic boundary of S. parvidens (Ditchfield, 2000). Besides, S. parvidens is supposedly widespread throughout Mesoamerica, whereas many other species of Sturnira have localized geographic ranges (Velazco and Patterson, 2013).

The geographical and phylogenetic uncertainties of S. parvidens represent an excellent opportunity to study recent diversification processes in the Mesoamerican lowlands, since it was suggested that this bat evolved after the emergence of the Isthmus of Panama during the Pleistocene (Velazco and Patterson, 2013). In other words, it is an ideal candidate for exploring the effect of Quaternary climatic oscillations on the process of Neotropical biota formation. We performed phylogenetic and phylogeographic analyses based on DNA sequences of mitochondrial and nuclear molecular markers (including samples of S. parvidens from throughout its geographic range, and samples of all species in Sturnira clade B), and comparison of climatic niches, to determine the processes of diversification in this lowland Mesoamerican bat. Our main goals were (1) to clarify the phylogenetic position of S. parvidens, (2) to determine whether S. parvidens show genetic breaks due to the action of Pleistocene climatic oscillations in the Mesoamerican lowlands, and (3) to analyze the role of climatic niche conservatism or divergence in the speciation process.

Section snippets

Taxon sampling and molecular protocols

We collected 54 specimens of S. parvidens in various states in Mexico following Mexico’s wildlife legislation (SEMARNAT SGPA/DGVS/11606/08257/06724). All material is deposited in the Mammal Collection of the Zoology Museum, UNAM (Facultad de Ciencias – Universidad Nacional Autónoma de México, Mexico City, Mexico, MZFC-M). In the analyses we also included samples of S. parvidens and related species, to clarify the inter-specific position of S. parvidens, from other scientific collections:

Sample sizes

We analyzed data from 1 sample of Vampyriscus bidens, and 312 individuals of the genus Sturnira: 62 samples correspond to S. aratathomasi, S. bidens, S. nana, and species from clade A; 77 individuals corresponded to S. angeli, S. bakeri, S. lilium, S. luisi, S. new species 3, and S. paulsoni; and 173 samples to S. parvidens. All sequences are available in Genbank (Supporting Information, Table S1).

We obtained a total of 1140 bp for cyt-b (394 variable and 330 informative sites); 392 bp (entire

Discussion

Molecular information is important in bats of the genus Sturnira because the relationships of these species cannot be clarified using a morphological perspective alone (Iudica, 2000, Pacheco and Patterson, 1991). In addition, morphological variation within the genus is subtle, and in some cases the characters used to diagnose different species have proven to be inconsistent (Jarrín-V and Clare, 2013).

Herein, we reported some relationships between the species of genus Sturnira that are different

Acknowledgements

We especially thank Bruce D. Patterson, Jorge Ortega, Luis Eguiarte, Adolfo G. Navarro-Sigüenza and two anonymous reviewers for comments and criticisms; and all the people who collected the samples in each scientific collection. Thanks to Celia López, Diego García, Robb Brumfield, Mark Hafner, Jesús Fernández, Francisco Durán, Robert Baker, Cibele Sotero, Burton Lim, Jacqueline Miller, and Jorge Ortega for providing samples. Thanks to the whole team at the MZFC-M and people who helped,

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