Abstract
Recent theories suggest that processes shaping species diversity are the same shaping genetic diversity, leading to a correlation between the two levels of diversity. Using Neotropical bat assemblages, and considering the genetic diversity of two co-distributed Chiroptera species with distinct life-history traits, Artibeus planirostris and Carollia perspicillata, we evaluated the correlation between metrics of taxonomic (species richness, evenness, and community divergence) and genetic diversity (number of haplotypes, haplotype diversity, allelic richness, expected heterozygosity and genetic divergence) in these two species. Landscape variables potentially affecting those correlations (distance to the nearest conservation unit, forest area, forest border length and number of forest fragments) were also analysed. For A. planirostris, we found a negative correlation between evenness and expected heterozygosity and also between mean presence-absence assemblage divergence and mean genetic divergence based on microsatellites. Our results indicate that the genetic diversity in A. planirostris is not explained by the landscape variables considered. For C. perspicillata, we found a positive correlation between species richness and haplotype richness and between evenness and expected heterozygosity. Genetic differentiation based on microsatellites in C. perspicillata was positively related to geographic distance and landscape differentiation. Allelic richness and expected heterozygosity in C. perspicillata were negatively related to distance from the conservation unit and forest area, but significance changed according to the spatial scale. We conclude that species-genetic diversity correlations may vary according to the species under study. Thus, A. planirostris appears to be ecologically different to other species in assemblages, while C. perspicillata seems to be ecologically similar.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Relevant data is contained in the paper, in the supplementary materials and in GenBank.
References
Anderson S (1997) Mammals of Bolivia, taxonomy and distribution. Bull Am Mus Nat Hist 231:1–652
Antonovics J (1976) The input from population genetics: “the new ecological genetics.” Syst Bot 1:233–245. https://doi.org/10.2307/2418718
Arnone IS, Trajano E, Pulchério-Leite A, Passos FC (2016) Long-distance movement by a great fruit-eating bat, Artibeus lituratus (Olfers, 1818), in southeastern Brazil (chiroptera, phyllostomidae): evidence for migration in neotropical bats? Biota Neotrop 16:1–6. https://doi.org/10.1590/1676-0611-BN-2015-0026
Baptista-Maria VR, Rodrigues RR, Damasceno Junior G, Maria FDS, Souza VC (2009) Composição florística de florestas estacionais ribeirinhas no estado de Mato Grosso do Sul, Brasil. Acta Bot Brasilica 23:535–548. https://doi.org/10.1590/S0102-33062009000200025
Bárquez RM, Giannini NP, Mares MA (1993) Guide to the bats of Argentina. Oklahome Museum of Natural History University of Oklahoma, Oklahoma
Bárquez RM, Mares MA, Braun JK (1999) Guide to the bats of Argentina. Museum of Texas Tech University, Lubbock
Bardeleben C, Campbell P, Lara M, Moore RL (2007) Isolation of polymorphic tetranucleotide microsatellite markers for the silky short-tailed bat Carollia brevicauda. Mol Ecol Notes 7(1):63–65. https://doi.org/10.1111/j.1471-8286.2006.01525.x
Blum MJ, Bagley MJ, Walters DM, Jackson SA, Daniel FB, Chaloud DJ, Cade BS (2012) Genetic diversity and species diversity of stream fishes covary across a land-use gradient. Oecologia 168(1):83–95. https://doi.org/10.1007/s00442-011-2078-x
Bonaccorso F, Winkelmann J, Shin D, Agrawal C, Aslami N, Bonney C, Hsu A, Jekielek P, Knox A, Kopach S, Jennings T, Lasky J, Menesale S, Richards J, Rutland J, Sessa A, Zhaurova L, Kunz T (2006) Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (phyllostomidae). Biotropica 39(2):249–256. https://doi.org/10.1111/j.1744-7429.2006.00251.x
Brosset A, Charles-Dominique P, Cockle A, Cosson JF, Masson D (1996) Bat communities and deforestation in French Guiana. Can J Zool 74(11):1974–1982. https://doi.org/10.1139/z96-224
Bruford M, Hanotte O, Brookfield J, Burke T (1992) Singlelocus and DNA fingerprinting. In: Howelzel A (ed) Molecular genetic analyses of populations: a practical approach. IRL Press, Oxford, pp 225–269
Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Carstens BC, Sullivan J, Davalos LM, Larsen PA, Pedersen SC (2004) Exploring population genetic structure in three species of Lesser Antillean bats. Mol Ecol 13(9):2557–2566. https://doi.org/10.1111/j.1365-294X.2004.02250.x
Cleary DFR, Fauvelot C, Genner MJ, Menken SBJ, Mooers A (2006) Parallel responses of species and genetic diversity to El Niño Southern oscillation-induced environmental destruction. Ecol Lett 9(3):301–307. https://doi.org/10.1111/j.1461-0248.2005.00876.x
Cleary KA, Waits LP, Hohenlohe PA (2016) Development and characterization of fourteen novel microsatellite markers for the chestnut short-tailed fruit bat (Carollia castanea), and cross-amplification to related species. PeerJ 4:e2465. https://doi.org/10.7717/peerj.2465
Cloutier D, Thomas D (1992) Carollia perspicillata. Mamm Species 417:1–9. https://doi.org/10.2307/3504157
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927–930
Esbérard C, Freitas G, Luz J, Costa L, Freitas L (2011) Intervalos máximos entre captura e recaptura de morcegos no estado do Rio de Janeiro, sudeste do Brasil. Chiropt Neotrop 17(1):957–962
Fischer E, Silveira M, Munin RL, Camargo G, Sanos CF, Ramos Pereira MJ, Fischer W, Eriksson A (2018) Bats in the dry and wet Pantanal. Hystrix 29(1):11–17. https://doi.org/10.4404/hystrix-00019-2017
Fleming TH (1988) The short-tailed fruit bat. The University of Chicago Press, Chicago
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Fox J (2007) The car package. R Foundation for Statistical Computing, Vienna
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Furtado P, Guimarães JG, Fonsar BC (1982) Vegetação. In: Levantamento de recursos naturais Folha SF-21-Campo Grande. Brasil, Ministério das Minas e Energia, Secretaria-Geral Projeto RADAMBRASIL 28:281–316
Gardner A (2007) Order chiroptera. In: Gardner A (ed) Mammals of South America. University Of Chicago Press, Chicago, pp 187–484
Gregorin R, Taddei VA (2002) Chave artificial para a identificaçao de molossídeos brasileiros (mammalia, chiroptera). Mastozool Neotrop 9:13–32
Hollis L (2005) Artibeus planirostris. Mamm Species 775:1–6. https://doi.org/10.1644/1545-1410(2005)775[0001:AP]2.0.CO;2
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography, monographs in population biology. Princeton University Press, Princeton, NJ
Hulce D, Li X, Snyder-Leiby T, Liu CJ (2011) GeneMarker® genotyping software: tools to increase the statistical power of DNA fragment analysis. J Biomol Tech: JBT 22(Suppl):S35
IBAMA (2000) Decreto s/n de 22 de setembro de 2000. http://www.planalto.gov.br/ccivil_03/DNN/2000/Dnn9037.htm
IBGE (2017) Censo Agro 2017. https://censos.ibge.gov.br/agro/2017/. Accessed 15 Feb 2017
Janzen D (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51. https://doi.org/10.1146/annurev.es.10.110179.000305
Kahilainen A, Puurtinen M, Kotiaho JS (2014) Conservation implications of species—genetic diversity correlations. Glob Ecol Conserv 2:315–323. https://doi.org/10.1016/j.gecco.2014.10.013
Kalko EKV, Handley C (2001) Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecol 153:319–333. https://doi.org/10.1023/A:1017590007861
Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15(2):173–190. https://doi.org/10.1046/j.1420-9101.2002.00377.x
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4(8):782–788. https://doi.org/10.1111/2041-210X.12067
Kim S (2015) ppcor: an R package for a fast calculation to semi-partial correlation coefficients. Commun Stat Appl Methods 22(6):665
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, New York
Klingbeil B, Willig MR (2009) Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. J Appl Ecol 46(1):203–213. https://doi.org/10.1111/j.1365-2664.2008.01594.x
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15(3):259–263. https://doi.org/10.1127/0941-2948/2006/0130
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Lamy T, Jarne P, Laroche F, Pointeier JP, Huth G, Segard A, David P (2013) Variation in habitat connectivity generates positive correlations between species and genetic diversity in a metacommunity. Mol Ecol 22(17):4445–4456. https://doi.org/10.1111/mec.12399
Lamy T, Laroche F, David P, Massol F, Jarne P (2017) The contribution of species–genetic diversity correlations to the understanding of community assembly rules. Oikos 126(6):759–771. https://doi.org/10.1111/oik.03997
Lino A, Fonseca C, Rojas D, Fischer E, Ramos Pereira MJ (2019) A meta-analysis of the effects of habitat loss and fragmentation on genetic diversity in mammals. Mamm Biol 94(1):69–76. https://doi.org/10.1016/j.mambio.2018.09.006
MacSwiney GMC, Clarke FM, Racey PA (2008) What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in neotropical bat assemblages. J Appl Ecol 45:1364–1371. https://doi.org/10.1111/j.1365-2664.2008.01531.x
Marinello MM, Bernard E (2014) Wing morphology of neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Can J Zool 92(2):141–147. https://doi.org/10.1139/cjz-2013-0127
Marinho-Filho J (1991) The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil. J Trop Ecol 7(1):59–67. https://doi.org/10.1017/S0266467400005083
Marques JT, Ramos Pereira MJ, Palmeirim JM (2012) Availability of food for frugivorous bats in Lowland Amazonia: the influence of flooding and of river banks. Acta Chiropt 14(1):183–194. https://doi.org/10.3161/150811012X654862
Martins MPV (2016) Área de uso seleção de habitat por Artibeus planirostris (Chiroptera: Phyllostomidae) no Pantanal. Universidade Federal de Mato Grosso do Sul, Campo Grande
Mato Grosso do Sul (2014) Avaliação ambiental estratégica do Prodetur Nacional de Mato Grosso do Sul. Mato Grosso do Sul, Campo Grande
Mazerolle MJ (2017) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.3-1, https://cran.r-project.org/package=AICcmodavg.
McCulloch ES, Stevens RD (2011) Rapid development and screening of microsatellite loci for Artibeus lituratus and their utility for six related species within Phyllostomidae. Mol Ecol Resour 11(5):903–913. https://doi.org/10.1111/j.1755-0998.2011.03027.x
McCulloch ES, Sebastián Tello J, Whitehead A, Rolõn-Mendoza CMJ, Maldonado-Rodríguez MCD, Stevens RD (2013) Fragmentation of Atlantic Forest has not affected gene flow of a widespread seed-dispersing bat. Mol Ecol 22(18):4619–4633. https://doi.org/10.1111/mec.12418
McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. University of Massachusetts, Amherst. Available at: http://www.umass.edu/landeco/research/fragstats/fragstats.html
Meyer CFJ, Kalko EKV, Kerth G (2009) Small-scale fragmentation effects on local genetic diversity in two phyllostomid bats with different dispersal abilities in Panama. Biotropica 41(1):95–102. https://doi.org/10.1111/j.1744-7429.2008.00443.x
Milton K, Windsor DM, Morrison DW, Estribi MA (1982) Fruiting phenologies of two Neotropical Ficus species. Ecology 63(3):752–762. https://doi.org/10.2307/1936796
Munin RL, Fischer E, Gonçalves F (2012) Food habits and dietary overlap in a phyllostomid bat assemblage in the Pantanal of Brazil. Acta Chiropt 14(1):195–204. https://doi.org/10.3161/150811012X654871
Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41(2):225–233. https://doi.org/10.1111/j.1469-1809.1977.tb01918.x
Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878. https://doi.org/10.1046/j.1365-2699.1999.00305.x
Odat N, Hellwig FH, Jetschke G, Fischer M (2010) On the relationship between plant species diversity and genetic diversity of Plantago lanceolata (Plantaginaceae) within and between grassland communities. J Plant Ecol 3(1):41–48. https://doi.org/10.1093/jpe/rtp017
Papadopoulou A, Anastasiou I, Spagopoulou F, Stalimerou M, Terzopoulou S, Legakis A, Vogler AP (2011) Testing the species–genetic diversity correlation in the Aegean Archipelago: toward a haplotype-based macroecology? Am Nat 178(2):241–255. https://doi.org/10.1086/660828
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Puşcaş M, Taberlet P, Choler P (2008) No positive correlation between species and genetic diversity in European alpine grasslands dominated by Carex curvula. Divers Distrib 14(5):852–861. https://doi.org/10.1111/j.1472-4642.2008.00489.x
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramos Pereira MJ, Marques JT, Palmeirim J (2010) Vertical stratification of bat assemblages in flooded and unflooded Amazonian forests. Curr Zool 56(4):469–478. https://doi.org/10.1093/czoolo/56.4.469
Raup D, Crick R (1979) Measurement of faunal similarity in paleontology. J Paleontol 53(5):1213–1227
Reis N, Peracchi A, Pedro W, Lima I (2007) Morcegos do Brasil. Univesidade Estadual de Londrina, Londrina
Ricklefs RE, Lovette IJ (1999) The roles of island area per se and habitat diversity in the species-area relationships of four Lesser Antillean faunal groups. J Anim Ecol 68(6):1142–1160. https://doi.org/10.1046/j.1365-2656.1999.00358.x
Ripperger SP, Tschapka M, Kalko EKV, Rodriguez-Herrera B, Mayer F (2012) Life in a mosaic landscape: anthropogenic habitat fragmentation affects genetic population structure in a frugivorous bat species. Conserv Genet 14(5):925–934. https://doi.org/10.1007/s10592-012-0434-y
Robinson JD, Diaz-Ferguson E, Poelchau MF, Pennings S, Bishop TD, Wares J (2010) Multiscale diversity in the marshes of the Georgia coastal ecosystems LTER. Estuar Coasts 33(4):865–877. https://doi.org/10.1007/s12237-009-9188-2
Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Shurin JB, Allen EG (2001) Effects of competition, predation, and dispersal on species richness at local and regional scales. Am Nat 158(6):624–637. https://doi.org/10.1086/323589
Silveira M, Tomas WM, Fischer E, Bordignon MO (2018) Habitat occupancy by Artibeus planirostris bats in the Pantanal wetland. Brazil Mamm Biol 91(1):1–6. https://doi.org/10.1016/j.mambio.2018.03.003
Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17(7):866–880. https://doi.org/10.1111/ele.12277
Struebig MJ, Kingston T, Petit EJ, Le Comber SC, Zubaid A, Mohd-Adnan A, Rossiter SJ (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecol Lett 14(6):582–590. https://doi.org/10.1111/j.1461-0248.2011.01623.x
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101(30):11030–11035. https://doi.org/10.1073/pnas.0404206101
Teixeira RC, Corrêa CE, Fischer E (2009) Frugivory by Artibeus jamaicensis (Phyllostomidae) bats in the Pantanal. Brazil Stud Neotrop Fauna Environ 44(1):7–15. https://doi.org/10.1080/01650520802692283
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vellend M (2003) Island biogeography of genes and species. Am Nat 162(3):358–365. https://doi.org/10.1086/377189
Vellend M (2004) Parallel effects of land-use history on species diversity and genetic of forest herbs. Ecology 85(11):3043–3055. https://doi.org/10.1890/04-0435
Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85(2):183–206. https://doi.org/10.1086/652373
Vellend M, Geber M (2005) Connections between species diversity and genetic diversity. Ecol Lett 8(7):767–781. https://doi.org/10.1111/j.1461-0248.2005.00775.x
Wehenkel C, Bergmann F, Gregorius HR (2006) Is there a trade-off between species diversity and genetic diversity in forest tree communities? Plant Ecol 185(1):151–161. https://doi.org/10.1007/s11258-005-9091-2
Wei X, Jiang M (2012) Contrasting relationships between species diversity and genetic diversity in natural and disturbed forest tree communities. New Phytol 193(3):779–786. https://doi.org/10.1111/j.1469-8137.2011.03957.x
Whitlock R (2014) Relationships between adaptive and neutral genetic diversity and ecological structure and functioning: a meta-analysis. J Ecol 102(4):857–872. https://doi.org/10.1111/1365-2745.12240
Acknowledgements
We thank José Quintero for help with the field sampling design and many volunteers for support during the field work, in particular, Alan Eriksson, Carol Santos, Mauricio Silveira and Guilli Silveira. We are thankful to the Foundation for Science and Technology (FCT/MCTES) for financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through Portuguese national funds. A. Lino was supported by the FCT/MCTES—POPHQREN, fellowship PD/BD/52566/2014. Eduardo Ferreira is funded by national funds (OE), through FCT- Foundation for Science and Technology, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the art. 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. E. Fischer and M.J. Ramos Pereira were supported by Productivity Grants by the National Council for Scientific and Technological Development (CNPq), Brazil and the FUNDECT/CAPES 44/2014 PAPOS-MS project. This study is part of the Long-Term Ecological Research Program—Serra da Bodoquena—maintained by CNPq, and implemented with funds from FUNDECT (Process 23/200.668/2013).
Author information
Authors and Affiliations
Contributions
All authors contributed for the study design and the writing of the manuscript. EF and AL conceived the field sampling design; AL collected the field data and did the laboratory analyses; EF, AL and MJRP performed the statistical analyses and discussed the results.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethical approval
Our study was conducted under the licenses 10615-1 from IBAMA and 41652-1 and 48146-1 from ICMBio.
Informed consent
All authors consent to participate in the manuscript.
Consent for publication
All authors have read the final version of the manuscript and approve its submission.
Additional information
Communicated by Karen E. Hodges.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lino, A., Ferreira, E., Fonseca, C. et al. Species–genetic diversity correlation in phyllostomid bats of the Bodoquena plateau, Brazil. Biodivers Conserv 30, 403–429 (2021). https://doi.org/10.1007/s10531-020-02097-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-020-02097-0