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

Abstract Background 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. In these studies, either sample sizes w...

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Main Authors: Ondine Filippi-Codaccioni, Marie-Pauline Beugin, Damien M. de Vienne, Elodie Portanier, David Fouchet, Cecile Kaerle, Lina Muselet, Guillaume Queney, Eric J. Petit, Corinne Regis, Jean-Baptiste Pons, Dominique Pontier
Format: Article
Language:English
Published: BMC 2018-11-01
Series:BMC Evolutionary Biology
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Online Access:http://link.springer.com/article/10.1186/s12862-018-1289-8
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author Ondine Filippi-Codaccioni
Marie-Pauline Beugin
Damien M. de Vienne
Elodie Portanier
David Fouchet
Cecile Kaerle
Lina Muselet
Guillaume Queney
Eric J. Petit
Corinne Regis
Jean-Baptiste Pons
Dominique Pontier
author_facet Ondine Filippi-Codaccioni
Marie-Pauline Beugin
Damien M. de Vienne
Elodie Portanier
David Fouchet
Cecile Kaerle
Lina Muselet
Guillaume Queney
Eric J. Petit
Corinne Regis
Jean-Baptiste Pons
Dominique Pontier
author_sort Ondine Filippi-Codaccioni
collection DOAJ
description Abstract Background 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. 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. Results A 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). Conclusions The 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.
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spelling doaj.art-bba858eb6c7d46729756e126394d347a2022-12-21T21:32:40ZengBMCBMC Evolutionary Biology1471-21482018-11-0118111310.1186/s12862-018-1289-8Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological dataOndine Filippi-Codaccioni0Marie-Pauline Beugin1Damien M. de Vienne2Elodie Portanier3David Fouchet4Cecile Kaerle5Lina Muselet6Guillaume Queney7Eric J. Petit8Corinne Regis9Jean-Baptiste Pons10Dominique Pontier11University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558ANTAGENE, Animal Genomics LaboratoryANTAGENE, Animal Genomics LaboratoryANTAGENE, Animal Genomics LaboratoryUMR ESE, Ecology and Ecosystem Health, INRA, Agrocampus OuestUniversity Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558University Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558Abstract Background 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. 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. Results A 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). Conclusions The 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.http://link.springer.com/article/10.1186/s12862-018-1289-8Pteronotus cf. parnelliiMicrosatelliteMitochondrial DNAPhylogenyEcholocationPopulation genetics
spellingShingle Ondine Filippi-Codaccioni
Marie-Pauline Beugin
Damien M. de Vienne
Elodie Portanier
David Fouchet
Cecile Kaerle
Lina Muselet
Guillaume Queney
Eric J. Petit
Corinne Regis
Jean-Baptiste Pons
Dominique Pontier
Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
BMC Evolutionary Biology
Pteronotus cf. parnellii
Microsatellite
Mitochondrial DNA
Phylogeny
Echolocation
Population genetics
title Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
title_full Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
title_fullStr Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
title_full_unstemmed Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
title_short Coexistence of two sympatric cryptic bat species in French Guiana: insights from genetic, acoustic and ecological data
title_sort coexistence of two sympatric cryptic bat species in french guiana insights from genetic acoustic and ecological data
topic Pteronotus cf. parnellii
Microsatellite
Mitochondrial DNA
Phylogeny
Echolocation
Population genetics
url http://link.springer.com/article/10.1186/s12862-018-1289-8
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