Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data

Ondine Filippi-Codaccioni,Guillaume Queney,Elodie Portanier,Lina Muselet,Marie-Pauline Beugin,Jean-Baptiste Pons,David Fouchet,Damien M De Vienne,Dominique Pontier,Eric J Petit,Corinne Regis,Cecile Kaerle

doi:10.1186/s12862-018-1289-8

Abstract

BackgroundThe distinction between lineages of neotropical bats from the Pteronotus parnellii species complex has been previously made according to mitochondrial DNA, and especially morphology and acoustics, in order to separate them into two species. In these studies, either sample sizes were too low when genetic and acoustic or morphological data were gathered on the same individuals, or genetic and other data were collected on different individuals. In this study, we intensively sampled bats in 4 caves and combined all approaches in order to analyse genetic, morphologic, and acoustic divergence between these lineages that live in the same caves in French Guiana.ResultsA multiplex of 20 polymorphic microsatellite markers was developed using the 454-pyrosequencing technique to investigate for the first time the extent of reproductive isolation between the two lineages and the population genetic structure within lineages. We genotyped 748 individuals sampled between 2010 and 2015 at the 20 nuclear microsatellite loci and sequenced a portion of the cytochrome c oxydase I gene in a subset of these. Two distinct, non-overlapping haplogroups corresponding to cryptic species P. alitonus and P. rubiginosus were revealed, in accordance with previous findings. No spatial genetic structure between caves was detected for both species. Hybridization appeared to be quite limited (0.1–4%) using microsatellite markers whereas introgression was more common (7.5%) and asymmetric for mitochondrial DNA (mtDNA).ConclusionsThe extremely low rate of hybridization could be explained by differences in life cycle phenology between species as well as morphological and acoustical distinction between sexes in one or the other species. Taken together, these results add to our growing understanding of the nature of species boundaries in Pteronotus parnelli, but deserve more in-depth studies to understand the evolutionary processes underlying asymmetric mtDNA introgression in this group of cryptic species.

Highlights

The distinction between lineages of neotropical bats from the Pteronotus parnellii species complex has been previously made according to mitochondrial Deoxyribonucleic acid (DNA), and especially morphology and acoustics, in order to separate them into two species
Nuclear genetic analysis We built a multiplex of 20 microsatellite markers (Additional file 1: Table S2)
These 20 microsatellite markers were successfully amplified for 748 bat samples with a mean amplification rate of 98.7%

Summary

Introduction

The distinction between lineages of neotropical bats from the Pteronotus parnellii species complex has been previously made according to mitochondrial DNA, and especially morphology and acoustics, in order to separate them into two species. The detection of cryptic species, i.e., genetically divergent species previously classified as a single species due to morphological similarity [1, 2], has significantly increased for all major terrestrial and aquatic taxonomic groups and across biogeographical regions [2, 3] through the use of large-scale DNA sequencing approaches such as DNA barcoding [4, 5] The discovery of this cryptic diversity has had profound implications for both evolutionary theory and future conservation decisions (see [6,7,8] for an example involving bats), especially in threatened ecosystems for which biodiversity has likely been underestimated. An example of this is Drosophila paulistorum for which semi-species are morphologically similar, but have different courtship song patterns [20]

Methods

Results

Discussion

Conclusion