Geographic variation of contact calls suggest distinct modes of vocal transmission in a leaf-roosting bat
Populations that have historically been isolated from each other are expected to differ in some heritable features. This divergence could be due to drift (and other mechanisms of neutral evolution) or differential adaptation of populations to local conditions. Discriminating between these two evolutionary trajectories can be difficult, but when possible, such data provides critical insight into the evolutionary history of a species. Here, we examine the patterns of geographic variation of two contact signals regularly produced by disc-winged bats, Thyroptera tricolor, and discuss possible processes leading to the observed patterns of differentiation. We compared allopatric populations separated by an elevational barrier, and estimated genetic distance using nuclear microsatellite loci. Our findings revealed that the mountain ridge is permeable to gene flow. Acoustic divergence was significantly explained by genetic and spatial factors, supporting the notion that stochastic factors are the main drivers of signal divergence. Yet, we found different patterns of geographic variation between the two types of calls. We examine how this variability in the patterns of acoustic divergence may suggest distinct modes of signal transmission within and between populations (i.e., social vs genetic transmission). This work provides further support of the role of random change shaping communication systems in mammals, and highlights the importance of studying multiple elements of a species repertoire to evaluate the underlying processes driving signal evolution.
Despite increasing interest in studying patterns of acoustic divergence, the relative contribution of adaptive and stochastic processes underlying variation of acoustic signals remain poorly understood, particularly in mammals. Our study examines signal divergence in Spix’s disc-winged bats, Thyoptera tricolor, with the goal of understanding the underlying processes driving signal evolution. Specifically, we studied whether the patterns of geographic variation of two social signals regularly emitted by T. tricolor are congruent with patterns of genetic distance among populations separated by a geographic barrier. We demonstrate that genetic and spatial distance explains acoustic variation, which points to stochastic processes as major drivers of signal divergence in T. tricolor. Notably, we found that the patterns of geographic variation differ between the two types of calls studied. We suggest that this variation results from distinct modes of vocal transmission within populations. Comparison of different signal types provides additional insight of social pressures shaping call design.
KeywordsContact calls Thyroptera tricolor Geographic barrier Vocal divergence Signal evolution Population genetic structure
We are indebted to Corcovado and Tortuguero National Park rangers and Aguilar family for housing and support in the field. We thank Genuar Núñez and Jairo Moya for assistance in the field, and Julian Schmid, Jackie Wrage, and Nicholas Johnson for their valuable help in video analysis. We would like to thank Gerald Wilkinson and two anonymous reviewers for their input on previous versions of the manuscript.
This research was supported by the National Science Foundation Grant # HRD-0811239 to the NDSU Advance FORWARD program, start-up funds from the Department of Biological Sciences and College of Science and Mathematics at NDSU (EHG), Sigma Xi Grants-in-Aid of Research Program (BKM), and the NDSU graduate school dissertation fellowship (BKM).
Compliance with ethical standards
All applicable international, national, and institutional guidelines for the care and use of animals were followed. This study was approved by the Costa Rican authorities (MINAE; SINAC; reference no. ATM-ACOSA-001-01, 034-2012; CONAGEBIO, reference no. R003-2011-OT) and by the NDSU Animal Care and Use Committee (Protocol no. A11022, A12052).
Conflict of interest
The authors declare that they have no conflict of interest.
- Baker MC (2000) Cultural diversification in the flight call of the ringneck parrot in Western Australia. Condor 102:905–910. https://doi.org/10.1650/0010-5422(2000)102[0905:CDITFC]2.0.CO;2Google Scholar
- Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecol 89:2623–2632Google Scholar
- Boughman JW, Rundle HD, Schluter D (2005) Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361–373. https://doi.org/10.1111/j.0014-3820.2005.tb00995.x CrossRefPubMedGoogle Scholar
- Cavalli-Sforza LL, Feldman MW (1981) Cultural transmission and evolution: a quantitative approach. Princeton University Press, PrincetonGoogle Scholar
- Fox J, Weisberg S (2011) An R companion to applied regression, eecond edition. Thousand Oaks CA: Sage. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion. Accessed 20 Jan 2015
- Hartshorn GS, Hammel BE (1994) Vegetation types and floristic patterns. In: McDade L, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a neotropical rain forest. The University of Chicago Press, Chicago. Illinois, USA, pp 73–89Google Scholar
- Herwitz SR (1981) Regeneration of selected tropical tree species in Corcovado National Park, Costa Rica. University of California Press, BekeleyGoogle Scholar
- Holdridge LR (1967) Life zone Ecology Tropical Science Center, San Jose, Costa RicaGoogle Scholar
- Legendre P., Borcard D., Blanchet G., Dray S (2012) MEM Spatial eigenfunction and principal coordinate analyses. http://r-forge.r-project.org/projects/sedar/. Accessed 20 Jan 2015
- Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K (2018) cluster: Cluster Analysis Basics and Extensions. R package version 2.0.7–1.Google Scholar
- Oksanen, J., Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara, RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: Community Ecology Package. R package version 2.3–0Google Scholar
- Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625. https://doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2Google Scholar
- Pröhl H, Koshy RA, Mueller U, Rand AS, Ryan MJ (2006) Geographic variation of genetic and behavioral traits in northern and southern túngara frogs. Evolution 60:1669–1679. https://doi.org/10.1111/j.0014-3820.2006.tb00511.x CrossRefPubMedGoogle Scholar
- Revelle W (2017) psych: Procedures for personality and psychological research, http://personality-project.org/r/psych-manual.pdf
- Savage JM, Heyer WR (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, Central America: with 6 figures. Stud Neotrop Fauna E 5:111–131Google Scholar
- Wilson DE (2008) Family Thyropteridae Miller 1907. In: Gardner AL (ed) Mammals of South America, vol. 1: Marsupials, xenarthrans, shrews and bats. University of Chicago Press, Chicago, pp 392–396Google Scholar