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Speciation Dynamics of the Fruit-Eating Bats (Genus Artibeus): With Evidence of Ecological Divergence in Central American Populations

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Bat Evolution, Ecology, and Conservation

Abstract

An increasing number of studies have identified complex diversification patterns of Neotropical faunal groups. One example of such complexity is found in bats of the widely distributed and locally abundant Neotropical genus Artibeus, wherein both allopatric and hybrid speciation events have been hypothesized. However, conflicting hypotheses regarding the timescale of diversification for Artibeus exist, and therefore, temporal inferences of the speciation events within the genus remain in doubt. We examine hypotheses regarding the chronology of diversification events within Artibeus. Our results indicate the most parsimonious time of origin for the genus was during the late Miocene to early Pliocene, with multiple speciation events during the early Pleistocene. Considering this evolutionary timescale, we revisit a century-old systematic debate regarding the status of Central American populations known as Artibeus lituratus intermedius. We present nuclear genetic data that indicate intermedius is distinct from lituratus and hypothesize that this distinction was ecologically driven, likely involved sympatry and reinforcement, and occurred during the late Pleistocene or early Holocene. Collectively, the data from Artibeus indicate that multiple speciation processes underlie extant levels of diversity within the genus. Our analyses provide further evidence for complex origins of the Neotropical fauna and contribute to a greater understanding of the natural processes underlying the origin of species.

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Acknowledgments

We thank R. D. Bradley for his valuable discussions throughout the stages of our investigation. C. Blair, H. H. Genoways, S. C. Pedersen, C. D. Phillips, C. J. Phillips, R. E. Strauss, and P. M. Velazco provided helpful comments. We are grateful to H. J. Garner, K. McDonald, and J. P. Carrera of the Natural Science Research Laboratory of the Museum of Texas Tech University for assistance with loans of tissue material. This study would not have been possible were it not for the collecting efforts of members of the 2001 and 2004 Sowell Expeditions to Ecuador and Honduras. We thank all researchers who have worked to generate the molecular data used herein. Financial support was provided by J. Sowell, A. Brown, the Texas Tech University Biological Database Program, and the American Society of Mammalogists.

Author information

Authors and Affiliations

  1. Department of Biology, Duke University, Durham, NC, 27708, USA

    Peter A. Larsen

  2. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409-3131, USA

    María R. Marchán-Rivadeneira & Robert J. Baker

Authors
  1. Peter A. Larsen
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  2. María R. Marchán-Rivadeneira
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  3. Robert J. Baker
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Corresponding author

Correspondence to Peter A. Larsen .

Editor information

Editors and Affiliations

  1. School of Biological Sciences, University of Northern Colorado, Greeley, Colorado, USA

    Rick A. Adams

  2. Department of Biology, South Dakota State, Brookings, South Dakota, USA

    Scott C. Pedersen

Appendices

Appendix A

Distribution maps of species of Artibeus following the data presented herein and in Webster and Jones (1983), Marques-Aguiar (2007), Genoways et al. (2010), Larsen et al. (2010a), and Larsen et al. (2010b). Species are arranged phylogenetically following Fig. 16.2. Plate 16.1: A. concolor, A. hirsutus, A. inopinatus, A. fraterculus, A. fimbriatus, A. aequatorialis, A. jamaicensis, and A. obscurus. Plate 16.2: A. lituratus, A. intermedius, A. schwartzi, A. planirostris, and A. amplus. The distribution of Artibeus sp. (sensu Redondo et al. 2008) remains to be determined.

Plate 16.1
figure 00168

Distribution maps of Artibeus concolor, A. hirsutus, A. inopinatus, A. fraterculus, A. fimbriatus, A. aequatorialis, A. jamaicensis, and A. obscurus

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Plate 16.2
figure 00169

Distribution maps of Artibeus lituratus, A. intermedius, A. schwartzi, A. planirostris, and A. amplus

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Appendix B

Specimens examined. Numbers associated with each specimen are enclosed in parentheses. Cytochrome-b sequences from Freygang (2006), Guerrero et al. (2004), Guerrero et al. (2008), Larsen et al. (2007), Larsen et al. (2010b), Redondo et al. (2008), and Van Den Bussche et al. (1998) and 16S ribosomal sequences from Hoofer et al. (2008). Distinct Brazilian cytochrome-b haplotypes from Redondo et al. (2008) were used in the mismatch distribution and Bayesian skyline plot analyses (GenBank accession numbers = EU160724–EU160833). TK = Tissue Number: Natural Science Research Laboratory of the Museum of Texas Tech University, Lubbock. GenBank accession numbers reported for all other sequences. * = used in AFLP analysis; † = used in molecular clock analyses, and ‡ = used in cytochrome-b haplotype network construction.

A. aequatorialis: Ecuador: El Oro (TK 135391*); Esmeraldas (TK 135701*), (TK 135702*), (TK 135905*), (TK 135906*); Guayas (TK 134602*); Loja (FJ179232†, FJ179186†, TK 135290*). A. concolor: Suriname: Sipaliwini (FJ179223†, FJ179173†). A. fraterculus: Ecuador: El Oro (TK 135408*), (TK 135226*), (TK 135760*); Guayas (DQ869389†, FJ179174†, TK 134686*), (TK 134950*), (TK 134947*). A. hirsutus: Mexico: Michoacan (FJ179226†, FJ179181†). A. inopinatus: Honduras: Valle (FJ179227†, FJ179177†, TK 101201*), (TK 101202*). A. intermedius: Costa Rica: Guanacaste (U66502‡). Honduras: Colon (TK 136293‡), (TK 136891*); Comayagua (TK 101269*), (AY684729, TK 101284*), (AY684730‡, TK 101285*), (TK 101938*), (TK 136052*‡), (TK 136027*); Copan (FJ179230‡, TK 101993*), (FJ179231); Valle (TK 101261*). Mexico: Morelos (AY144338‡), Veracruz (AY144339‡); Panama: Bocas del Toro (AY684737‡). A. jamaicensis: Jamaica, St. Ann’s Parish (DQ869480†, FJ179187†, TK 27682*), (TK 27686*), (TK 27691*). Honduras: Atlantida (TK 101763*), (TK 101381*); Copan (TK 101997*); Olancho (TK 102059*). A. lituratus: Brazil: Acre (EU160800‡); Amazonas (EU160761‡); Bahia (EU160725‡); Espirito Santo (EU160740‡), (EU160745‡), (EU160794‡); Maranhao (EU160827‡); Mato Grosso (EU160798‡); Minas Gerais (EU160724‡), (EU160799‡), (EU160814‡), (EU160815‡), (EU160817‡), (EU160822‡); Piaui (EU160829‡), (EU160830‡); Rio de Janeiro (AY684735‡), (EU160729‡), (EU160733‡); Santa Catarina (DQ985483‡), (DQ985485‡); Sao Paulo (AY684736‡), (EU160803‡), (EU160826‡). Ecuador: Esmeraldas (DQ869393‡), (TK 104643‡), (TK 104644*); Pastaza (FJ179233†‡, FJ179194†, TK 104112*), (AY684732‡), (AY684733‡), (TK 104333‡), (TK 104427‡), (TK 104441‡). Grenada: Carriacou (GQ861668‡). Guyana (TK 86512‡). Honduras: Atlantida (TK 101404*); Colon (TK 136258*), (TK 136293‡), (TK 136294*), (TK 136297*), (TK 136788*), (TK 136809*), (TK 136810*); Comayagua (TK 136075*). Paraguay: Dept. Canindeyu (TK 99645*); Dept. San Pedro (TK 56994*). Panama: Bocas del Toro (AY684731‡). St. Vincent and the Grenadines: Union Island (FJ179234‡, TK 128642*), (TK 128643*), (GQ861670‡). Suriname: Brokopondo (AY684740‡). Trinidad and Tobago: Trinidad (U66505‡). A. obscurus: Ecuador: Pastaza (TK 104001*), (TK 104310*). Suriname: Nickerie (FJ179185†); Para (U66506). Guyana (FJ179235†, FJ179184†). A. planirostris: Venezuela: Guarico (DQ869424†, FJ179189†, TK 15013*), Barinas (TK 19024*). Ecuador: Pastaza (TK 104413*), (TK 104414*), (TK 104406*), (TK 104410*), (TK 104411*), (TK 104419*). A. schwartzi: St. Vincent and the Grenadines: St. Vincent (DQ869524†, FJ179193†). Dermanura phaeotis: Mexico: Chiapas (FJ179245†, FJ179218†). D. rosenbergi: Ecuador: Esmeraldas (FJ179258†, FJ179219†). D. tolteca: Honduras: Comayagua (FJ179258†, FJ179216†). D. watsoni: Honduras: Colon (FJ179259†, FJ179205†). Ectophylla alba: Costa Rica: Limon (AY157033†, AY395811†). Enchisthenes hartii: Peru: Cusco (AY395838†); Huanuco (U66517†).

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Larsen, P.A., Marchán-Rivadeneira, M.R., Baker, R.J. (2013). Speciation Dynamics of the Fruit-Eating Bats (Genus Artibeus): With Evidence of Ecological Divergence in Central American Populations. In: Adams, R., Pedersen, S. (eds) Bat Evolution, Ecology, and Conservation. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7397-8_16

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