Abstract
The habitat first rule (HFR) proposes that radiating species initially diversify into habitat specialists and later into dietary specialists within a given habitat, whereas the general vertebrate model (GVM) adds divergence of sexually selected traits as a possible third axis of specialization subsequent to habitat and dietary divergence. In this study, using 12 Miniopterus spp. from Madagascar we test predictions of the HFR and GVM from ecological and evolutionary perspectives on Grinnellian and Eltonian niche structures. We used environmental niche models (ENMs) to quantify the Grinnellian niche, both for current and last inter-glacial climates. We used null models to examine Eltonian niche patterns of sympatric species in terms of their phylogenetic relatedness and phenotypic and sensory characters associated with the trophic niche—body size, skull morphology and echolocation. As predicted by the HFR, we found evidence for labile Grinnellian niches: there was no similarity in ENMs between sister species; overlap in ENMs was significantly low in >65 % of all possible species pairs; there was no relationship between ENM niche overlap and phylogenetic distances between species; and there was no phylogenetic signal in suitable bioclimatic zones among species. Conversely, we found equivocal support for the HFR regarding Eltonian niche patterns. Closely related species tended to be distributed among ensembles rather than within ensembles, although there was no evidence for overdispersion in phylogenetic patterns in ensembles. In <50 % of the observed combinations of sympatric Miniopterus spp., we found significant signal for overdispersion of phenotypic and sensory characters. We hypothesize that selective processes associated with the adaptive radiation of Miniopterus spp. on Madagascar may have favoured bats to diversify first into broad scale habitat specialists, but argue that understanding the relative influence of bionomic processes at a local spatial scale will require more reciprocal comparisons of Eltonian niches.
Similar content being viewed by others
References
Ackerly DD, Schwilk DW, Webb CO (2006) Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 87:S50–S61
Adler PB, HilleRisLambers J, Levine JM (2007) A niche for neutrality. Ecol Lett 10:95–104
Ahmadzadeh F, Flecks M, Carretero MA et al (2013) Rapid lizard evolution lacking niche conservatism: ecological diversification within a complex landscape. J Biogeogr 40:1807–1818
Aldridge H, Rautenbach IL (1987) Morphology, echolocation and resource partitioning in insectivorous bats. J Anim Ecol 56:763–778
Alfaro ME, Santini F, Brock C et al (2009) Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Nat Acad Sci USA 106:13410–13414
Andreas M, Reiter A, Benda P (2012) Dietary composition, resource partitioning and trophic niche overlap in three forest foliage-gleaning bats in central Europe. Acta Chiropterol 14:335–345
Araújo MB, Guisan A (2006) Five (or so) challenges for species distribution modelling. J Biogeogr 33:1677–1688
Arita H (1997) Species composition and morphological structure of the bat fauna of Yucatan, Mexico. J Anim Eco 66:83–97
Barclay RMR, Fullard JH, Jacobs DS (1999) Variation in the echolocation calls of the hoary bat (Lasiurus cinereus): influence of body size, habitat structure, and geographic location. Can J Zool 77:530–534
Bloch CP, Stevens RD, Willig MR (2011) Body size and resource competition in New World bats: a test of spatial scaling laws. Ecography 34:460–468
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioural traits are more labile. Evolution 57:717–745
Bogdanowicz W, Fenton MB, Daleszczyk K (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. J Zool 247:381–393
Bohmann K, Monadjem A, Lehmkuhl Noer C et al (2011) Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing. PLoS ONE 6:e21441
Boria RA, Olson LE, Goodman SM et al (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77
Boumans L, Vieites DR, Glaw F et al (2007) Geographical patterns of deep mitochondrial differentiation in widespread Malagasy reptiles. Mol Phylogenet Evol 45:822–839
Bull CM (1991) Ecology of parapatric distributions. Annu Rev Ecol Syst 22:19–36
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366
Christidis L, Goodman SM, Naughton K et al (2014) Insights into the evolution of a cryptic radiation of bats: dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae). PLoS ONE 9:e92440
Colwell RK, Rangel TF (2009) Hutchinson’s duality: the once and future niche. Proc Natl Acad Sci USA 106:19651–19658
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts
Darriba D, Taboada GL, Doallo R et al (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
Devictor V, Clavel J, Julliard R et al (2010) Defining and measuring ecological specialization. J Appl Ecol 47:15–25
Drummond AJ, Suchard MA, Xie D et al (2013) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol and Evol 29:1969–1973
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Ann Rev Ecol Evol Syst 40:677–697
Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151
Esselstyn JA, Maher SP, Brown RM (2011) Species interactions during diversification and community assembly in an island radiation of shrews. PLoS ONE 6:e21885
Fauth JE, Bernardo J, Camara M et al (1996) Simplifying the jargon of community ecology: a conceptual approach. Am Nat 147:282–286
Fitzpatrick BM, Turelli M (2006) The geography of mammalian speciation: mixed signals from phylogenies and range maps. Evolution 60:601–615
Freeman PW (1998) Form, function, and evolution in skulls and teeth of bats. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithsonian Institution Press, Washington, DC, pp 140–156
Garcia LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663
Gautier L, Goodman SM (2008) Introduction à la flore. In: Goodman SM (ed) Paysages naturels et biodiversité de Madagascar. Muséum national d’Histoire naturelle, Paris, pp 103–140
Glor RE (2010) Phylogenetic insights on adaptive radiation. Annu Rev Ecol Evol Syst 41:251–270
Goodman SM (2011) Les chauves-souris de Madagascar. Association Vahatra, Antananarivo
Goodman SM, Ryan KE, Maminirina CP et al (2007) Specific status of populations on Madagascar referred to Miniopterus fraterculus (Chiroptera: Vespertilionidae), with description of a new species. J Mammal 88:1216–1229
Goodman SM, Bradman HM, Maminirina CP et al (2008) A new species of Miniopterus (Chiroptera: Miniopteridae) from lowland southeastern Madagascar. Mamm Biol 73:199–213
Goodman SM, Maminirina CP, Bradman HM et al (2009a) The use of molecular phylogenetic and morphological tools to identify cryptic and paraphyletic species: examples from the diminutive long-fingered bats (Chiroptera: Miniopteridae: Miniopterus) on Madagascar. Am Mus Novit 3669:1–34
Goodman SM, Maminirina CP, Weyeneth N et al (2009b) The use of molecular and morphological characters to resolve the taxonomic identity of cryptic species: the case of Miniopterus manavi (Chiroptera, Miniopteridae). Zool Scr 38:339–363
Goodman SM, Maminirina CP, Bradman HM et al (2010) Patterns of morphological and genetic variation in the endemic Malagasy bat Miniopterus gleni (Chiroptera: Miniopteridae), with the description of a new species, M. griffithsi. J Zool Syst Evol Res 48:75–86
Goodman SM, Ramasindrazana B, Maminirina CP et al (2011) Morphological, bioacoustical, and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species. Zootaxa 2880:1–19
Gotelli NJ, Entsminger GL (2012) EcoSim: null models software for ecology. Version 7.7 Kesey-Bear
Hancock L, Edwards EJ (2014) Phylogeny and the inference of evolutionary trajectories. J Exp Bot 65:3491–3498
Hastie T, Fithian W (2013) Inference from presence-only data; the ongoing controversy. Ecography 36:864–867
Heller K-G, Helversen OV (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80:178–186
Hijmans RJ, Graham CH (2006) The ability of climate envelope models to predict the effect of climate change on species distributions. Glob Change Biol 12:2272–2281
Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Jiménez-Valverde A, Lira-Noriega A, Peterson AT et al (2010) Marshalling existing biodiversity data to evaluate biodiversity status and trends in planning exercises. Ecol Res 25:947–957
Jønsson KA, Fabre P-H, Fritz SA et al (2012) Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. Proc Nat Acad Sci USA 109:6620–6625
Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behaviour, ecology and life history. P Roy Soc Lond B Bio 368:20120341
Kamilar JM, Muldoon KM (2010) The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PLoS ONE 5:e11073
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Kingston T, Jones G, Zubaid A et al (2000) Resource partitioning in rhinolophoid bats revisited. Oecologia 124:332–342
Kozak KH, Wiens JJ (2010) Niche conservatism drives elevational diversity patterns in Appalachian salamanders. Am Nat 176:40–54
Kramer-Schadt S, Niedballa J, Pilgrim J et al (2013) The importance of correcting for sampling bias in MaxEnt species distribution models. Div Distr 19:1366–1379
Lack D (1947) Darwin’s finches. Cambridge University Press, Cambridge
Lam MM-Y, Martin-Creuzburg D, Rothhaupt K-O et al (2013) Tracking diet preference of bats using stable isotope and fatty acid signatures of faeces. PLoS ONE 8:e83452
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analyses. J Stat Soft 25:1–18
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1007
Losos JB (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat 175:623–639
Losos JB, Glor RE, Kolbe JJ et al (2006) Adaptation, speciation, and convergence: a hierarchical analysis of adaptive radiation in Caribbean Anolis lizards. Ann Missouri Bot Gard 93:24–33
Mackey BG, Lindenmayer DB (2001) Towards a hierarchical framework for modelling the spatial distribution of animals. J Biogeogr 28:1147–1166
Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. Available from http://mesquiteproject.org (Accessed March 2014)
Maddison WP, Slatkin M (1991) Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45:1184–1197
Mahler DL, Revell LJ, Glor RE et al (2010) Ecological opportunity and the rate of morphological evolution in the diversification of greater Antillean anoles. Evolution 64:2731–2745
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093
Moat J, Smith P (2007) Atlas of the vegetation of Madagascar. Royal Botanic Gardens, Kew
Monadjem A, Taylor PJ, Cotterill FPD et al (2010) Bats of central and southern Africa: a biogeographic and taxonomic synthesis. Wits University Press, Johannesburg
Monadjem A, Goodman SM, Stanley WT et al (2013) A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters. Zootaxa 3746:123–142
Muldoon KM, Goodman SM (2010) Ecological biogeography of Malagasy non-volant mammals: community structure is correlated with habitat. J Biogeogr 37:1144–1159
Münkemüller T, Lavergne S, Bzeznik B et al (2012) How to measure and test phylogenetic signal. Methods Ecol Evol 3:743–757
Orozco-terWengel P, Nagy ZT, Vieites DR et al (2008) Phylogeography and phylogenetic relationships of Malagasy tree and ground boas. Biol J Linn Soc 95:640–652
Otto-Bliesner BL, Marshall SJ, Overpeck JT et al (2006) Simulating arctic climate warmth and ice field retreat in the Last Interglaciation. Science 311:1751–1753
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Pearson RG, Raxworthy CJ, Nakamura M et al (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34:102–117
Perneger TV (1998) What’s wrong with Bonferroni adjustments. BMJ 316:1236–1238
Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267
Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Puechmaille SJ, Allegrini B, Benda P et al (2014) A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa. Zootaxa 3794:108–124
R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org (Accessed July 2014)
Rainho A, Palmerin JM (2011) The importance of distance to resources in the spatial modelling of bat foraging habitat. PLoS ONE 6:e19227
Ramasindrazana B, Goodman SM, Schoeman MC et al (2011) Identification of cryptic species of Miniopterus bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and morphological characters. Biol J Linn Soc 104:284–302
Rambaut A, Drummond AJ (2007) Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer (Accessed March 2014)
Raxworthy CJ, Ingram CM, Rabibisoa N et al (2007) Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Syst Biol 56:907–923
Razgour O, Clare EL, Zeale MRK et al (2011) High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecol Evol 1:556–570
Reddy S, Driskell A, Rabosky DL et al (2012) Diversification and the adaptive radiation of the vangas of Madagascar. Proc Royal Soc B 279:2062–2071
Reding DM, Foster JT, James HF et al (2009) Convergent evolution of “creepers” in the Hawaiian honeycreeper radiation. Biol Lett 5:221–224
Revell L (2012) Phylogenetic signal on very small trees. Phylogenetic tools for comparative biology. Available from http://blog.phytools.org/2012/09/phylogenetic-signal-on-very-small-trees.html (Accessed 14 September 2013)
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Sallan LC, Friedman M (2012) Heads or tails: staged diversification in vertebrate evolutionary radiations. Proc R Soc B 279:2025–2032
Schatz GE (2000) Endemism in the Malagasy tree flora. In: Lourenço WR, Goodman SM (eds) Diversité et endémisme à Madagascar. Mémoires de la Société de Biogéographie, Paris
Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64
Schluter D (2000a) Ecological character displacement in adaptive radiation. Am Nat 156:S4–S16
Schluter D (2000b) The ecology of adaptive radiation. Oxford University Press, New York
Schoeman MC, Jacobs DS (2003) Support for the allotonic frequency hypothesis in an insectivorous bat community. Oecologia 134:154–162
Schoeman MC, Jacobs DS (2008) The relative influence of competition and prey defenses on the phenotypic structure of insectivorous bat ensembles in southern Africa. PLoS ONE 3:e3715
Schoeman MC, Jacobs DS (2011) The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles. Oecologia 166:493–506
Schoeman MC, Waddington KJ (2011) Do deterministic processes influence the phenotypic patterns of animalivorous bat ensembles at urban rivers? Afr Zool 46:288–301
Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. P Roy Soc Lond B Bio 273:1987–1998
Sexton JP, McIntyre PJ, Angert AL et al (2009) Evolution and ecology of species range limits. Annu Rev Ecol Syst 40:415–436
Smith TB, Wayne RK, Girman DJ et al (1997) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857
Soberón J (2007) Grinnellian and eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123
Stevens RD (2011) Relative effects of time for speciation and tropical niche conservatism on the latitudinal diversity gradient of phyllostomid bats. P Roy Soc Lond B Bio 278:2528–2536
Stevens RD, Willig MR (1999) Size assortment in New World bat communities. J Mammal 80:644–658
Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends Ecol Evol 18:126–131
Swets J (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293
Vences M, Glaw F (2002) Molecular phylogeography of Boophis tephraeomystax: a test case for east-west vicariance in Malagasy anurans. Spixiana 25:79–84
Vences M, Wollenberg KC, Vieites DR et al (2009) Madagascar as a model region of species diversification. Trends Ecol Evol 24:456–465
Villalobos F, Arita HT (2010) The diversity field of New World leaf-nosed bats (Phyllostomidae). Global Ecol Biogeogr 19:200–211
Warren DL (2012) In defense of ‘niche modeling’. Trends Ecol Evol 27:497–500
Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883
Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611
Webb C, Ackerly D, McPeek M et al (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Whittaker R, Willis K, Field R (2001) Scale and species richness: towards a general, hierarchical theory of species diversity. J Biogeogr 28:453–470
Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology and conservation biology. Annu Rev Evol Syst 36:519–539
Wiens JJ, Ackerly DD, Allen AP et al (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324
Willig MR, Mares MA (1989) A comparison of bat assemblages from phytogeographic zones of Venezuela. In: Morris DW, Abramsky Z, Fox BJ, Willig MR (eds) Patterns in the structure of mammalian communities. Texas Tech University, Lubbock, pp 59–67
Wilmé L, Goodman SM, Ganzhorn J (2006) Biogeographic evolution of Madagascar’s microendemic biota. Science 312:1063–1065
Wisz MS, Hijmans RJ, Li J et al (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14:763–773
Wollenberg KC, Vieites DR, van der Meijden A et al (2008) Patterns of endemism and species richness in Malagasy cophylin frogs support a key role of mountainous areas for speciation. Evolution 62:1890–1907
Wollenberg KC, Vieites DR, Glaw F et al (2011) Speciation in little: the role of range and body size in the diversification of Malagasy mantellid frogs. BMC Evol Biol 11:217
Yoder AD, Heckman KL (2006) Mouse lemur phylogeography revises a model of ecogeographic constraint in Madagascar. In: Fleagle J, Lehman SM (eds) Primate biogeography. Springer, New York, pp 255–268
Yoder AD, Nowak MD (2006) Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu Rev Ecol Evol Syst 37:405–431
Yoder JB, Clancey E, Des Roches S et al (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23:1581–1596
Acknowledgments
We thank the Direction Générale de l’Environnement et des Forêts and Madagascar National Parks for providing authorizations for the capture, collection and exportation of animals under a protocol of collaboration between the Département de Biologie Animale (Université d’Antananarivo), Association Vahatra and the Field Museum of Natural History. Financial support for the fieldwork associated with this project was graciously given by the John D. and Catherine T. MacArthur Foundation and Volkswagen Foundation. Access to computing and storage facilities owned by parties and projects contributing to the Czech National Grid Infrastructure MetaCentrum, provided under the programme “Projects of Large Infrastructure for Research, Development, and Innovations” (LM2010005), is greatly appreciated. Two anonymous reviewers made valuable comments on a previous version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schoeman, M.C., Goodman, S.M., Ramasindrazana, B. et al. Species interactions during diversification and community assembly in Malagasy Miniopterus bats. Evol Ecol 29, 17–47 (2015). https://doi.org/10.1007/s10682-014-9745-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-014-9745-4