Ecological niche differentiation among Aztec fruit-eating bat subspecies (Chiroptera: Phyllostomidae) in Mesoamerica

Authors

  • Iván Hernández-Chávez Universidad Nacional Autónoma de México
  • Lázaro Guevara Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México.
  • Joaquín Arroyo-Cabrales Laboratorio de Arqueozoología, Subdirección de Laboratorios y Apoyo Académico, Instituto Nacional de Antropología e Historia.
  • Livia León-Paniagua Museo de Zoología “Alfonso L. Herrera”, Facultad de Ciencias, Universidad Nacional Autónoma de México.

Keywords:

Geographic barriers, Mesoamerica, neotropical bats, niche divergence, ecological speciation.

Abstract

Artibeus aztecus is a Mesoamerican montane bat with three currently recognized, allopatric subspecies. No study has evaluated the phylogenetic status of the subspecies. However, through an analysis of its ecological niche and its geographic distribution, here we analyze whether there is differentiation of the climatic requirements for each subspecies, assessing whether niche evolution is a potential factor in subspecies differentiation. We assayed ecological niche models for each subspecies, analyzed the response curves for the most important climatic variables of each model, and generated the potential distribution model for each subspecies. We assayed a background similarity test between the subspecies to determine how similar their niches were. We found differences in climatic requirements for the three allopatric subspecies and the most important variables and their response curves. Potential distribution models concur with Mesoamerican highlands and highlight the lowlands of the isthmus of Tehuantepec and the Nicaraguan depression as possible geographic barriers. Differences found between ecological niches for each subspecies contrast with previous findings for the species and other phyllostomid bats. Niche conservatism may have caused geographic isolation in the past, and differences in environmental requirements may have appeared later. Molecular and morphological analyses are necessary to clarify the taxonomic status of these populations and the evolutionary processes involved in their diversification.

References

AGUILAR, J. M. 2019. Geographic distribution analysis of the genus Xenodacnis (Birds: Thraupidae) using ecological niche modeling. Revista Peruana de Biologia 26:317–324.

AIELLO-LAMMENS, M. E., ET AL. 2015. spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38:541-545.

ANDERSEN, K. 1906. LXI .— Brief diagnoses of a new genus and ten new froms of Stenodermatous bats. Journal of Natural History Series 7 18:419–423.

ARBELÁEZ-CORTÉS, E., Á. S. NYÁRI, AND A. G. NAVARRO-SIGÃœENZA. 2010. The differential effect of lowlands on the phylogeographic pattern of a Mesoamerican montane species (Lepidocolaptes affinis, Aves: Furnariidae). Molecular Phylogenetics and Evolution 57:658–668.

ARNONE, I. S., ET AL. 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 Neotropica 16:1–6.

ARRIBAS, P., ET AL. 2013. Integrative taxonomy and conservation of cryptic beetles in the Mediterranean region (Hydrophilidae). Zoologica Scripta 42:182–200.

BAKER, R. J., AND R. D. BRADLEY. 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87:643–662.

BAKER, R. J., ET AL. 2016. Higher level classification of Phyllostomid bats with a summary of DNA synapomorphies. Acta Chiropterologica 18:1–38.

BARVE, N., ET AL. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222:1810–1819.

BLAIR, C., ET AL. 2019. Cryptic diversity in the Mexican highlands: Thousands of UCE loci help illuminate phylogenetic relationships, species limits and divergence times of montane rattlesnakes (Viperidae: Crotalus). Molecular Ecology Resources 19:349–365.

BORIA, R. A., ET AL. 2014. Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecological Modelling 275:73–77.

BRIONES, M., ET AL., 2019. Responses of phyllostomid bats to traditional agriculture in Neotropical montane forests of Southern Mexico. Zoological Studies 58:e9.

BRYSON, R. W., ET AL. 2018. Phylogenomic insights into the diversification of salamanders in the Isthmura bellii group across the Mexican highlands. Molecular Phylogenetics and Evolution 125:78–84.

BUERMANN, W., ET AL. 2008. Predicting species distributions across the Amazonian and Andean regions using remote sensing data. Journal of Biogeography 35:1160–1176.

BURGIN, C. J., ET AL. 2018. How many species of mammals are there? Journal of Mammalogy 99:1–14.

CAMPBELL, L., ET AL. 2015. Climate change influences on global distributions of dengue and chikungunya virus vectors. Philosophical Transactions of the Royal Society B: Biological Sciences 370:20140135.

CASTAÑEDA-RICO, S. S. 2005. Variación geográfica de Dermanura azteca (Chiroptera: Phyllostomidae) en la República Mexicana (Bachelor thesis). Universidad Nacional Autónoma de México.

CASTOE, T. A., ET AL. 2009. Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. Journal of Biogeography 36:88–103.

CERÓN-HERNÁNDEZ, J. A., ET AL. 2022. Diversidad, tipos de dieta de murciélagos y su respuesta a bordes de bosque mesófilo de montaña, Veracruz, México. Ecosistemas y Recursos Agropecuarios 9:e3110.

CIRRANELLO, A., ET AL. 2016. Morphological diagnoses of higher-level Phyllostomid taxa (Chiroptera: Phyllostomidae). Acta Chiropterologica 18:39–71.

COBOS, M. E, ET AL. 2019. kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ:1–15.

DATZMANN, T., O. VON HELVERSEN, AND F. MAYER. 2010. Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evolutionary Biology 10:1–14.

DAVIS, W. B. 1969. A review of the small fruit bats (genus Artibeus) of Middle America. The Southwestern Naturalist 14:15–29.

DAZA, J. M., T. A. CASTOE, AND C. L. PARKINSON. 2010. Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America. Ecography 33:343–354.

DINIZ-FILHO, J. A. F., ET AL. 2010. Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence. Global Ecology and Biogeography 19:916–926.

ESCOBAR, L. E., ET AL. 2014. Potential for spread of the white-nose fungus (Pseudogymnoascus destructans) in the Americas: Use of Maxent and NicheA to assure strict model transference. Geospatial Health 9:221–229.

FITZPATRICK, B. M., AND M. TURELLI. 2006. The geography of mammalian speciation: mixed signals from phylogenies and range maps. Evolution 60:601–615.

GASCON, C., ET AL. 2000. Riverine barriers and the geographic distribution of Amazonian species. Proceedings of the National Academy of Sciences of the United States of America 97:13672–13677.

GEHRING, P. S., ET AL. 2012. The influence of riverine barriers on phylogeographic patterns of Malagasy reed frogs (Heterixalus). Molecular Phylogenetics and Evolution 64:618–632.

GUEVARA, L., AND V. SÁNCHEZ-CORDERO. 2018. Patterns of morphological and ecological similarities of small-eared shrews (Soricidae, Cryptotis) in tropical montane cloud forests from Mesoamerica. Systematics and Biodiversity:1–14.

GUTIÉRREZ-GARCÍA, T. A., AND E. VÁZQUEZ-DOMÍNGUEZ. 2013. Consensus between genes and stones in the biogeographic and evolutionary history of Central America. Quaternary Research (United States) 79:311–324.

HEINICKE, M. P., T. R. JACKMAN, AND A. M. BAUER. 2017. The measure of success: geographic isolation promotes diversification in Pachydactylus geckos. BMC Evolutionary Biology 17:1–17.

HENDING, D. 2021. Niche-separation and conservation biogeography of Madagascar’s fork-marked lemurs (Cheirogaleidae: Phaner): Evidence of a new cryptic species? Global Ecology and Conservation 29:e01738.

HERNÁNDEZ-CANCHOLA, G. 2018. Diversificación de dos especies del género Sturnira (Chiroptera: Phyllostomidae) en Mesoamérica (PhD thesis). Universidad Nacional Autónoma de México.

HIJMANS, R. J., ET AL. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965–1978.

HOOFER, S. R., ET AL. 2008. Phylogenetics of the fruit-eating bats (Phyllostomidae: Artibeina) inferred from mitochondrial DNA sequences. Occasional Papers, Museum of Texas Tech University:1–15.

JIMÉNEZ, R. A., AND J. F. ORNELAS. 2016. Historical and current introgression in a Mesoamerican hummingbird species complex: a biogeographic perspective. PeerJ 2016.

JORDANO, P., ET AL. 2011. Frugivores and seed dispersal: mechanisms and cosequences for biodiversity of a key ecological interaction. Biology Letters 7:321-323.

KRAKER-CASTAÑEDA, C., ET AL. 2017. Responses of phyllostomid bats to forest cover in upland landscapes in Chiapas southeast Mexico. Studies on Neotropical Fauna and Environment: 1-10.

KOZAK, K. H., C. H. GRAHAM, AND J. J. WIENS. 2008. Integrating GIS-based environmental data into evolutionary biology. Trends in Ecology and Evolution 23:141–148.

KOZAK, K. H., AND J. J. WIENS. 2006. Does niche conservatism promote speciation? a case study in North American salamanders. Evolution 60:2604–2621.

LENTZ, D. L., R. BYE, AND V. SÁNCHEZ-CORDERO. 2008. Ecological niche modeling and distribution of wild sunflower (Helianthus annuus L.) in Mexico. International Journal of Plant Sciences 169:541–549.

LEÓN-PANIAGUA, L., ET AL. 2007. Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Molecular Phylogenetics and Evolution 42:653–664.

LÓPEZ-GONZÁLEZ, C., AND D. F. GARCÍA-MENDOZA. 2006. Murciélagos de la Sierra Tarahumara, Chihuahua, México. Acta Zoológica Mexicana 22:109-135.

LORENZO, C., ET AL. 2017. Diversidad y conservación de los mamíferos terrestres de Chiapas, México. Revista Mexicana de Biodiversidad 88:735–754.

MARTÍNEZ-GORDILLO, D., O. ROJAS-SOTO, AND A. ESPINOSA DE LOS MONTEROS. 2010. Ecological niche modelling as an exploratory tool for identifying species limits: An example based on Mexican muroid rodents. Journal of Evolutionary Biology 23:259–270.

MEDINA-VAN BERKUM, P., ET AL. 2020. Community of bats in Cusco National Park, Honduras, a Mesoamerican Cloud Forest, including new regional and altitudinal records. Neotropical Naturalist 3:1–24.

MONTEIRO, L. R., AND M. R. NOGUEIRA. 2011. Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Evolutionary Biology 11:1–23.

MORALES-MARTÍNEZ, D. M., H. F. LÓPEZ-ARÉVALO, AND M. VARGAS-RAMÍREZ. 2021. Beginning the quest: Phylogenetic hypothesis and identification of evolutionary lineages in bats of the genus Micronycteris (Chiroptera, Phyllostomidae). ZooKeys 1028:135–159.

MUSCARELLA, R., ET AL. 2014. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5:1198–1205.

OSORIO-OLVERA, L., ET AL. 2020. ntbox: An R package with graphical user interface for modelling and evaluating multidimensional ecological niches. Methods in Ecology and Evolution 11:1199–1206.

OWEN, R. D. 1987. Phylogenetic analyses of the bat subfamily Stenodermatinae (Mammalia: Chiroptera). Special Publications of the Museum Texas Tech University 26:1–65.

PARRA-OLEA, G., ET AL. 2012. Isolation in habitat refugia promotes rapid diversification in a montane tropical salamander. Journal of Biogeography 39:353–370.

PEIXOTO, F. P., F. VILLALOBOS, AND M. V. CIANCIARUSO. 2017. Phylogenetic conservatism of climatic niche in bats. Global Ecology and Biogeography 26:1055–1065.

PETERSON, A. T., ET AL. 2008. Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling 213:63-72

PETERSON, A. T., ET AL. 2011. Ecological niches and geographic distributions. Princeton University Press, New Jersey.

PETERSON, A. T., M. PAPEŞ, AND M. EATON. 2007. Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550–560.

PETERSON, A. T., J. SOBERÓN, AND V. SÁNCHEZ-CORDERO. 1999. Conservatism of ecological niches in evolutionary time. Science 285:1265–1267.

PHILLIPS, S. J., R. P. ANDERSON, AND R. E. SCHAPIRE. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190:231–259.

PINEDA-LIZANO, W., AND G. CHAVERRI. 2022. Spatio-temporal distribution and reproductive phenology of Neotropical bat species in an altitudinal gradient in Costa Rica. Mammalian Biology 102:1–12.

PUEBLA-OLIVARES, F., ET AL. 2008. Speciation in the emerald toucanet (Aulacorhynchus prasinus) complex. The Auk 125:39–50.

PYRON, R. A., ET AL. 2015. Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biological Reviews 90:1248–1262.

REDONDO, R. A. F., ET AL. 2008. Molecular systematics of the genus Artibeus (Chiroptera: Phyllostomidae). Molecular Phylogenetics and Evolution 49:44–58.

RISSLER, L. J., AND J. J. APODACA. 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Systematic Biology 56:924–942.

ROBERTS, T. E. 2006. Multiple levels of allopatric divergence in the endemic Philippine fruit bat Haplonycteris fischeri (Pteropodidae). Biological Journal of the Linnean Society 88:329–349.

RODRÍGUEZ-CORREA, H., ET AL. 2015. How are oaks distributed in the neotropics? A perspective from species turnover, areas of endemism, and climatic niches. International Journal of Plant Sciences 176:222–231.

RODRÍGUEZ-GÓMEZ, F., C. GUTIÉRREZ-RODRÍGUEZ, AND J. F. ORNELAS. 2013. Genetic, phenotypic and ecological divergence with gene flow at the Isthmus of Tehuantepec: the case of the azure-crowned hummingbird (Amazilia cyanocephala). Journal of Biogeography 40:1360–1373.

RODRÍGUEZ-GÓMEZ, F., ET AL. 2021. Phylogeography, morphology and ecological niche modelling to explore the evolutionary history of Azure-crowned Hummingbird (Amazilia cyanocephala, Trochilidae) in Mesoamerica. Journal of Ornithology 162:529–547.

SALDAÑA-VÁZQUEZ, R. A. 2014. Intrinsic and extrinsic factors affecting dietary specialization in Noeotropical frugivorous bats. Mammal Review 44:215–224.

SCHOENER, T. W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726.

SEGURA-TRUJILLO, C. A., AND S. NAVARRO-PÉREZ. 2010. Escenario y problemática de conservación de los murciélagos (Chiroptera) cavernícolas del Complejo Volcánico de Colima, Jalisco-Colima, México. Therya 1:189–206.

SOBERÓN, J., AND M. NAKAMURA. 2009. Niches and distributional areas: concepts, methods and assumptions. Proceedings of the National Academy of Sciences 106:19644–19650.

SOLARI, S., ET AL. 2009. Operational criteria for genetically defined species: analysis of the diversification of the small fruit-eating bats, Dermanura (Phyllostomidae: Stenodermatinae). Acta Chiropterológica 11:279–288.

SOLARI, S., ET AL. 2019. Family Phyllostomidae. Pp. 444-583, in Handbook of the Mammals of the World - Volume 9. Bats (Wilson, D. E., and R. A. Mittermeier, eds.). Lynx Edicions. Barcelona, Spain.

STEVENS, R. D. 2006. Historical processes enhance patterns off diversity along latitudinal gradients. Proceedings of the Royal Society B: Biological Sciences 273:2283–2289.

STEVENS, R. D. 2011. Relative effects of time for speciationand tropical niche conservatism on the latitudinal diversity gradient of phyllostomid bats. Proceedings of the Royal Society B: Biological Sciences 278:2528–2536.

SULLIVAN, ARELLANO, AND ROGERS. 2000. Comparative phylogeography of Mesoamerican highland rodents: concerted versus independent response to past climatic fluctuations. The American Naturalist 155:755.

TOCCHIO, L. J., R., ET AL. 2015. Niche similarities among white-eared opossums (Mammalia, Didelphidae): Is ecological niche modelling relevant to setting species limits? Zoologica Scripta 44:1–10.

TORRES-MORALES, L. 2019. Límites de distribución actual de Sturnira hondurensis. Revista Mexicana de Biodiversidad 90:1–9.

TURELLI, M., N. H. BARTON, AND J. A. COYNE. 2001. Theory of Speciation. Trends in Ecology and Evolution 16:330–343.

WANG, B. C., AND T. B. SMITH. 2002. Closing the seed dispersal loop. Trends in Ecology and Evolution 17:379–386.

WARREN, D. L., ET AL. 2021. ENMTools 1.0: an R package for comparative ecological biogeography. Ecography 44:1-8.

WARREN, D. L., R. E. GLOR, AND M. TURELLI. 2008. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883.

WARREN, D. L., R. E. GLOR, AND M. TURELLI. 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611.

WIENS, J. J., AND C. H. GRAHAM. 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics 36:519–539.

ZAMORA-MEJÍAS, D., AND B. RODRÍGUEZ-HERRERA. 2017. Murciélagos (Chiroptera) del bosque premontano de San Ramón, Costa Rica. Revista Pnesamiento Actual 17:105–113.

ZINK, R. M. 2012. The geography of speciation: case studies from birds. Evolution: Education and Outreach 5:541–546.

Downloads

Published

2023-01-27

Issue

Section

Special Contribution