Abstract
Cryptic animal species are often distinguishable by nonvisual communication signals used in specific-mate recognition. The three cryptic taxa comprising the Paragalago zanzibaricus species complex use distinct loud calls that do not obviously reflect molecular phylogenetic relationships. Paragalago granti and P. cocos both have incremental calls but are not sister taxa; P. cocos is the sister taxon to P. zanzibaricus, which has a rolling (trilling) call like that of P. rondoensis, one of the outliers to the complex. To test current hypotheses of species delimitation, I conducted 378 playback trials, using conspecific and heterospecific loud calls and recording both vocal responses and movement toward the speaker. To investigate the sensory drive hypothesis (acoustic adaptation), I measured reverberation duration of 215 short “yap” mobbing calls and examined 282 sonotopes (local soundscapes). I tested the hypothesis that different species’ ear lengths allow the animals to filter out interfering frequencies in local background noise. On Zanzibar Island, P. zanzibaricus responded solely to conspecific calls (23/32). In South Africa, P. granti individuals responded to conspecific calls (12/22) but also sometimes to P. cocos calls (9/22). In Kenya, P. cocos individuals responded to conspecific calls (34/40) but also sometimes to P. zanzibaricus calls (8/40). The three habitats showed differences in reverberation duration, and soundscapes differed in background orthopteran frequencies. Incremental calls probably evolved in the ancestor of the complex, in response to high levels of reverberation and a continuous backdrop of katydid stridulation in dry forest. Secondary evolution of trilling and decreased ear size probably evolved as result of decreased reverberation and higher frequency katydid interference in the P. cocos–P. zanzibaricus ancestor. A loss of short units in P. zanzibaricus probably occurred as result of decreased reverberation in thicket. The study validates the three species of the complex and provides information supporting speciation by sensory drive.
Similar content being viewed by others
References
Ambrose, L. (2003). Three acoustic forms of Allen’s galagos (Primates: Galagonidae) in the Central Africa region. Primates, 44, 25–39. https://doi.org/10.1007/s10329-002-0004-x.
Bearder, S. K., Honess, P. E., & Ambrose, L. (1995). Species diversity among galagos with special reference to mate recognition. In L. Alterman, G. A. Doyle, & M. K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 331–352). Plenum Press.
Bearder, S. K., Honess, P. E., Bayes, M., Ambrose, L., & Anderson, M. (1996). Assessing galago diversity: A call for help. African Primates, 2(1), 11–15.
Bobe, R. (2006). The evolution of arid ecosystems in eastern Africa. Journal of Arid Environments, 66, 564–584. https://doi.org/10.1016/j.jaridenv.2006.01.010.
Boscolo, D., Metzger, J., & Vieillard, J. M. E. (2006). Efficiency of playback for assessing the occurrence of five bird species in Brazilian Atlantic Forest fragments. Anais da Academia Brasiliera de Ciências, 78(4), 629–644. https://doi.org/10.1590/S0001-37652006000400003.
Braune, P., Schmidt, S., & Zimmermannn, E. (2008). Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus spp.). BMC Biology, 6, 19. https://doi.org/10.1186/1741-7007-6-19.
Brown, C., Gomez, R., & Waser, P. (1995). Old world monkey vocalizations: Adaptation to the local habitat? Animal Behaviour, 50, 945–961. https://doi.org/10.1016/0003-3472(95)80096-4.
Burgess, N. D., & Clarke, G. P. (2000). The coastal forests of eastern Africa. IUCN.
Butynski, T. M, Kingdon, J. & Kalina, J. (2013). Mammals of Africa. II: Primates. Bloomsbury.
Charles-Dominique, P. (1977). Ecology and behaviour of nocturnal primates: Prosimians of equatorial West Africa. Duckworth.
Cracraft, J. (1983). Species concepts and speciation analysis. Current Ornithology, 1, 159–187.
Cummings, M. E., & Endler, J. A. (2018). 25 years of sensory drive: The evidence and its watery bias. Current Zoology, 64, 471–484. https://doi.org/10.1093/cz/zoy043.
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083.
Dobzhansky, T. (1937). Genetics and the origin of species. Columbia University Press.
Eldredge, N. (1993). What, if anything, is a species? In W. H. Kimbel & L. B. Martin (Eds.), Species, species concepts and primate evolution (pp. 3–20). Plenum Press.
Endler, J. A. (1992). Sensory drive: Does sensory biology bias or constrain the direction of evolution? The American Naturalist, 139, S1–S153.
Endler, J. A. (1993). Some general comments on the evolution and design of animal communication systems. Philosophical Transactions of the Royal Society B: Biological Sciences, 340, 215–225.
Endler, J. A., & Basolo, A. L. (1998). Sensory ecology, receiver biases and sexual selection. Trends in Ecology and Evolution, 13(10), 415–420. https://doi.org/10.1016/S0169-5347(98)01471-2.
Farina, A. (2014). Soundscape ecology: Principles, patterns, methods and applications. Dordrecht: Springer Science+Business Media. https://doi.org/10.1007/978-94-007-7374-5.
Ferguson, J. W. H. (2002). On the use of genetic divergence for identifying species. Biological Journal of the Linnean Society, 75, 509–516. https://doi.org/10.1046/j.1095-8312.2002.00042.x.
Fischer, J., Noser, R., & Hammerschmidt, K. (2013). Bioacoustic field research: A primer to acoustic analyses and playback experiments with primates. American Journal of Primatology, 75, 643–663. https://doi.org/10.1002/ajp.22153.
Freeman, B. G., & Montgomery, G. A. (2017). Using song playback experiments to measure species recognition between geographically isolated populations: A comparison with acoustic trait analyses. The Auk, 134, 867–870. https://doi.org/10.1642/AUK-17-63.1.
Génin, F., Yokwana, A., Kom, N., Couette, S., Dieuleveut, T., Nash, S. D., & Masters, J. C. (2016). A new galago species for South Africa (Primates: Strepsirhini, Galagidae). African Zoology, 51, 135–143. https://doi.org/10.1080/15627020.2016.1232602.
Groves, C. P. (2000). The genus Cheirogaleus: Unrecognized biodiversity in dwarf lemurs. International Journal of Primatology, 21, 943–961.
Groves, C. P. (2012). Species concept in primates. American Journal of Primatology, 74, 687–691. https://doi.org/10.1002/ajp.22035.
Groves, C. P. (2013). The nature of species: A rejoinder to Zachos et al. Mammalian Biology, 78, 7–9. https://doi.org/10.1016/j.mambio.2012.09.009.
Jones, H. G., Koka, K., Thornton, J. L., & Tollin, D. J. (2011). Concurrent development of the head and pinnae and the acoustical cues to sound location in a precocious species, the chinchilla (Chinchilla lanigera). Journal of the Association for Research in Otolaryngology, 12, 127–140. https://doi.org/10.1007/s10162-010-0242-3.
Jordan, E. A., Areta, J. I., & Holtzmann, I. (2017). Mate recognition systems and species limits in a warbling finch complex (Poospiza nigrorufa/whitii). Emu, 117(4), 344–358. https://doi.org/10.1080/01584197.2017.1360746.
Kacholi, D. S. (2018). Floristic similarity and diversity gradients in the Eastern Arc and coastal forests of Tanzania. Journal of Education, Humanities and Sciences, 7(2), 93–104.
Kirkwood, D., & Midgley, J. J. (1999). The floristics of sand forest in northern KwaZulu-Natal, South Africa. Bothalia, 29, 293–304.
Krause, B. (1993). The niche hypothesis: A virtual symphony of animal sounds; the origins of musical expression and the health of habitats. Soundscapes Newsletter, 6, 6–10.
Lei, R., Frasier, C. L., Hawkins, M. T., Engberg, S. E., Bailey, C. A., et al (2017). Phylogenomic reconstruction of sportive lemurs (genus Lepilemur) recovered from mitogenomes with inferences for Madagascar biogeography. Journal of Heredity, 108(2), 107–119. https://doi.org/10.1093/jhered/esw072.
Masters, J. C. (1991). Loud calls of Galago crassicaudatus and G. garnettii and their relation to habitat structure. Primates, 32, 153–167. https://doi.org/10.1007/BF02381173.
Masters, J. C. (1993). Primates and paradigms: problems with the identification of genetic species. In W. H. Kimbel & L. B. Martin (Eds.), Species, species concepts and primate evolution (pp. 43–64). Plenum Press.
Masters, J. C. (2000). The role of selection in speciation. In R. S. Singh & C. B. Krimbas (Eds.), Evolutionary genetics: From molecules to morphology (pp. 513–531). Cambridge University Press.
Masters, J. C., & Bragg, N. P. (2000). Morphological correlates of speciation in bush babies. International Journal of Primatology, 21(5), 793–813. https://doi.org/10.1023/A:1005590524932.
Masters, J. C., & Couette, S. (2015). Characterizing cryptic species: A morphometric analysis of craniodental characters in the dwarf galago genus Galagoides. American Journal of Physical Anthropology, 158, 288–299. https://doi.org/10.1002/ajpa.22792.
Masters, J. C., & Génin, F. (2018). The recognition concept of species, decades on. Theoretical Biology Forum, 111, 93–97. https://doi.org/10.19272/201811402010.
Masters, J. C., Génin, F., Couette, S., Groves, C. P., DelPero, M., & Pozzi, L. (2017). A new genus for the eastern dwarf galagos (Primates: Galagidae). Zoological Journal of the Linnean Society, 181, 229–241. https://doi.org/10.1093/zoolinnean/zlw028.
Mayr, E. (1982). Processes of speciation in animals. In C. Barigozzi (Ed.), Mechanisms of speciation (pp. 1–19). Alan R. Liss.
Mayr, E. (1988). The why and how of species. Biology and Philosophy, 3, 431–441. https://doi.org/10.1007/BF00647963.
Mayr, E. (1996). What is a species, and what is not? Philosophy of Science, 63, 262–277.
McGregor, P. K. (2000). Playback experiments: Design and analysis. Acta Ethologica, 3, 3–8. https://doi.org/10.1007/s102110000023.
Mendelson, T. C., & Shaw, K. L. (2012). The mis-(concept) of species recognition. Trends in Ecology and Evolution, 27(8), 421–427. https://doi.org/10.1016/j.tree.2012.04.001.
Mitani, J. C., & Stuht, J. (1998). The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission. Primates, 39, 171–182. https://doi.org/10.1007/BF02557729.
Mittermeier, R. A., Louis Jr., E. E., Richardson, M., Schwitzer, C., Langrand, O., et al (2010). Lemurs of Madagascar (3rd ed.). Arlington, VA: Conservation International.
Nietsch, A., & Kopp, M. L. (1998). Role of vocalization in species differentiation of Sulawesi tarsiers. Folia Primatologica, 69(1), 371–378. https://doi.org/10.1159/000052725.
Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., et al (2007). The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution, 43(1), 309–327. https://doi.org/10.1016/j.ympev.2006.10.026.
Paterson, H. E. H. (1985). The recognition concept of species. In E. S. Vrba (Ed.), Species and speciation (pp. 21–29). Pretoria, South Africa: Transvaal Museum Monograph No. 4.
Paterson, H. E. H. (1993). Evolution and the recognition concept of species. Baltimore: Johns Hopkins University Press.
Pijanowski, B. C., Villanueva-Rivera, L. J., Dumyahn, S. L., Farina, A., Krause, B. L., et al (2011). Soundscape ecology: The science of sound in the landscape. BioScience, 61, 203–216. https://doi.org/10.1525/bio.2011.61.3.6.
Pozzi, L. (2016). The role of forest expansion in species diversification among galagos (Primates: Galagidae). Journal of Biogeography, 43(10), 1930–1941. https://doi.org/10.1111/jbi.12846.
Pozzi, L., Disotell, T. R., Bearder, S. K., Karlsson, J., Perkin, A., & Gamba, M. (2019). Species boundaries within morphologically cryptic galagos: Evidence from acoustic and genetic data. Folia Primatologica, 90, 1–21. https://doi.org/10.1159/000496972.
Pozzi, L., Roos, C., & Blair, M. E. (2020). Molecular advances in lorisid taxonomy and phylogeny. In K. A. I. Nekaris & A. M. Burrows (Eds.), Evolution, ecology and conservation of lorises and pottos (pp. 57–66). Cambridge: Cambridge University Press.
Rasoloarison, R. M., Goodman, S. M., & Ganzhorn, J. U. (2000). Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology, 21, 963–1019.
Rosti, H., Pihlström, H., Bearder, S., Pellikka, P., & Rikkinen, J. (2020). Taxonomic inferences from vocalizations of nocturnal arboreal mammals of montane forests of the Taita Hills, Kenya. Diversity, 12(12), 473. https://doi.org/10.3390/d12120473.
Schüßler, D., Blanco, M., Salmona, J., Poelstra, J., Andriambeloson, J., et al (2020). Ecology and morphology of mouse lemurs (Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species. American Journal of Primatology, 82(9), e23180. https://doi.org/10.1002/ajp.23180.
Setchell, J. M. (2019). How to design, conduct and report primatological research. Cambridge: Cambridge University Press.
Sullivan, B. K. (2009). Mate recognition, species boundaries and the fallacy of “species Recognition”. The Open Zoology Journal, 2, 86–90. https://doi.org/10.2174/1874336600902010086.
Tattersall, I. (2013). Species level diversity among Malagasy lemurs. In J. C. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead: Advances in prosimian biology (pp. 11–20). New York: Springer Science+Business Media. https://doi.org/10.1007/978-1-4614-4511-1_2.
Truax, B., & Barrett, G. W. (2011). Soundscape in a context of acoustic and landscape ecology. Landscape Ecology, 26, 1201. https://doi.org/10.1007/s10980-011-9644-9.
Waser, P. M., & Brown, C. H. (1986). Habitat acoustics and primate communication. American Journal of Primatology, 10, 135–154. https://doi.org/10.1002/ajp.1350100205.
Waser, P. M., & Waser, M. (1977). Experimental studies of primate vocalization: Specializations for long-distance propagation. Journal of Comparative Ethology, 43, 239–263. https://doi.org/10.1111/j.1439-0310.1977.tb00073.x.
Wiens, J. J. (2004). What is speciation and how should we study it? The American Naturalist, 163, 914–923. https://doi.org/10.1086/386552.
Yoder, A. D., Rasoloarison, R. M., Goodman, S. M., Irwin, J. A., Atsalis, S., et al (2000). Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Proceedings of the National Academy of Sciences of the USA, 97(21), 11325–11330.
Zimmermannn, E. (1990). Differentiation of vocalizations in bushbabies (Galaginae) and the significance for assessing phylogenetic relationships. Zeitschrift für Zoologische Systematik und Evolutionsforschung, 28, 217–239.
Zimmermann, E. (2013). Primate serenades: Call variation, species diversity and adaptation in nocturnal strepsirhines. In J. C. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead: Advances in prosimian biology (pp. 287–295). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media. https://doi.org/10.1007/978-1-4614-4511-1_32.
Zimmermannn, E., Vorobieva, E., Wrogemann, D., & Hafen, T. (2000). Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). International Journal of Primatology, 21, 837–852.
Acknowledgments
I dedicate this article to the memories of Profs. Hugh Paterson and Maarten de Wit. I thank Warren Miller for the map and Judith Masters, as well as four anonymous reviewers, for their useful comments. AEON and the Iphakade Earth Stewardship Science Programme (Nelson Mandela University) provided essential support that allowed me to conduct this project. Finally, I thank Shirley Bethune, Catherine Hanekom, Kalama Kitsao, Nokuthula Kom, Leonard Muller, Lydia Muthoni, David Roberts, and Ayabulela Yokwana for their helps with this project. The National Research Foundation, South Africa, provided funding (Grant 93924).
Author information
Authors and Affiliations
Contributions
FG is the sole author of the paper that he conceived, designed and wrote.
Corresponding author
Additional information
Handling Editor: Joanna Setchell.
Rights and permissions
About this article
Cite this article
Génin, F. Speciation by Sensory Drive in the Paragalago zanzibaricus Species Complex. Int J Primatol 42, 478–498 (2021). https://doi.org/10.1007/s10764-021-00213-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-021-00213-7