Advertisement

The Relative Roles of Selection and Drift in Phenotypic Variation: Some Like It Hot, Some Like It Wet

  • David S. Jacobs
  • Gregory L. Mutumi
Chapter

Abstract

Acoustic signals mediate important functions, e.g. orientation, foraging and communication, that impact on the survival and reproduction of animals. The propagation of acoustic signals is also known to be influenced by habitat, particularly differences in climate. It is therefore likely that the environment would exert significant influence on such signals and that selection rather than drift would be largely responsible for geographic variation in acoustic signals. We investigated the role of selection and drift in geographic variation in the echolocation of two species of horseshoe bats Rhinolophus damarensis and R. clivosus (Rhinolophidae) with wide geographic distributions across the arid and mesic biomes of southern Africa. In both species, selection was found to be the dominant evolutionary process influencing phenotypic variation; however, there was evidence of drift in R. clivosus. Furthermore, selection was not differentially exerted across populations because there was no change in the results when localities were excluded one at a time. Population divergence appeared to be mediated by selection on traits associated with manoeuvrability, detection and size in both species despite their disparate distributions. However, the climatic factor that best explained geographic variation in echolocation was dependent on the biomes occupied by the species. Temperature was the dominant climatic factor in R. damarensis, a species with a largely arid distribution. In R. clivosus, a species with distributions across both mesic and arid biomes, temperature and relative humidity together explained variation in echolocation.

Notes

Acknowledgements

We thank Pierre Pontarotti for inviting us to contribute to this volume. We are grateful to many people who helped with sample collection and logistics in the field particularly, Prof. Peter Mundy of the National University of Science and Technology, Dr. H. Madzikanda of the Zimbabwe Parks and Wildlife Authority, Tinyiko Maluleke, Blessing Buleya, Reason Nyengera, Orsila Smit, Megan Cunnama, Ellenor Salo, Lizelle Odendaal, Serena Doole and Nyasha Gondo. Special thanks to Eugene Marais who provided invaluable information on Namibian bat roosts and the Namibian Ministry of Environment and Tourism and the Northern Cape for permission to do this research. For guidance in statistical analysis and editing the R script, we thank Rebecca Ackermann and Andrew Conith. This research was supported by grants to DSJ from the University of Cape Town and the South African Research Chair Initiative of the Department of Science and Technology, administered by the National Research Foundation (GUN 64798).

References

  1. Ackermann RR, Cheverud JM (2002) Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation. Am J Phys Anthropol 117:260–217Google Scholar
  2. Ackermann RR, Cheverud JM (2004) Detecting genetic drift versus selection in human evolution. Proc Natl Acad Sci 101:17946–17951Google Scholar
  3. Anthony ELP (1988) Age determination in bats. In: Kunz TH (ed) Ecological and behavioural methods for the study of bats. Smithsonian Institution Press, Washington D.C., pp 47–58Google Scholar
  4. Bastian A, Jacobs DS (2015) Listening carefully: increased perceptual acuity for species discrimination in multispecies signalling assemblages. Anim Behav 101:141–154Google Scholar
  5. Betti L, Balloux F, Hanihara T, Manica A (2010) The relative role of drift and selection in shaping the human skull. Am J Phys Anthropol 141:76–82Google Scholar
  6. Brandon RN (2005) The difference between selection and drift: a reply to Millstein. Biol Philos 20:153–170Google Scholar
  7. Brandon RN, Carson S (1996) The indeterministic character of evolutionary theory: no “no hidden variables proof” but no room for determinism either. Philos Sci 63:315–337Google Scholar
  8. Campbell P, Pasch B, Pino JL, Crino OL, Phillips M, Phelps SM (2010) Geographic variation in the songs of neotropical singing mice: testing the relative importance of drift and local adaptation. Evolution 64:1955–1972Google Scholar
  9. Chen S-F, Jones G, Rossiter SJ (2009) Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Proc R Soc B 276:3901–3909Google Scholar
  10. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Sunderland, Sunderland, MAGoogle Scholar
  11. Csorba G, Ujhelyi P, Thomas N (2003) Horseshoe bats of the world: (Chiroptera: Rhinolophidae). Alana Books, BerkshireGoogle Scholar
  12. de Azevedo S, Quinto-Sánchez M, Paschetta C, González-José R (2015) The first human settlement of the New World: a closer look at craniofacial variation and evolution of early and late Holocene Native American groups. Quat Int 431:152–167Google Scholar
  13. Dool SE, Puechmaille SJ, Foley NM, Allegrini B, Bastian A, Mutumi GL, Maluleke T, Odendaal LJ, Teeling EC, Jacobs DS (2016) Nuclear introns outperform mtDNA in phylogenetic reconstruction: lessons from horseshoe bats (Rhinolophidae: Chiroptera). Mol Phylogenet Evol 97:196–212Google Scholar
  14. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20Google Scholar
  15. Fenton MB (1999) Describing the echolocation calls and behaviour of bats. Acta Chiropterol 1(2):127–136Google Scholar
  16. Findley JS, Wilson DE (1982) Ecological significance of chiropteran morphology. In: Kunz TH (ed) Ecology of bats. Boston University Press, Boston, pp 243–260Google Scholar
  17. Finger NM, Bastian A, Jacobs DS (2017) To seek or speak? Dual function of an acoustic signal limits its versatility in communication. Anim Behav 127:135e152Google Scholar
  18. Freeman PW, Lemen CA (2010) Simple predictors of bite force in bats: the good, the better and the better still. J Zool 282:284–290Google Scholar
  19. Griffin DR (1958) Listening in the dark. Yale University Press, New HavenGoogle Scholar
  20. Irwin DE, Thimgan MP, Irwin JH (2008) Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role for stochasticity in signal evolution? J Evol Biol 21:435–448Google Scholar
  21. Jacobs DS, Barclay RMR, Walker MH (2007) The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia 152:583–594Google Scholar
  22. Jacobs DS, Babiker H, Bastian A, Kearney T, van Eeden R, Bishop JM (2013) Phenotypic convergence in genetically distinct lineages of a Rhinolophus species complex (Mammalia, Chiroptera). Plos ONE 8(12):e82614.  https://doi.org/10.1371/journal.pone.0082614
  23. Jacobs DS, Bastian A, Bam L (2014) The influence of feeding on the evolution of sensory signals: a comparative test of an evolutionary trade-off between masticatory and sensory functions of skulls in southern African Horseshoe bats (Rhinolophidae). J Evolut Biol 27:2829–2840Google Scholar
  24. Jacobs DS, Mutumi GL, Maluleke T, Webala PW (2016) Convergence as an evolutionary trade-off in the evolution of acoustic signals: echolocation in horseshoe bats as a case study. In: Pontarotti P (ed) Evolutionary biology: convergent evolution, evolution of complex traits, concepts and methods. Springer Interntaional Publishing, Switzerland, pp 89–103Google Scholar
  25. Jacobs DS, Catto S, Mutumi GL, Finger N, Webala PW (2017) Testing the sensory drive hypothesis: geographic variation in echolocation frequencies of Geoffroy’s horseshoe bat (Rhinolophidae: Rhinolophus clivosus). Plos ONE 12(11):e0187769.  https://doi.org/10.1371/journal.pone.0187769
  26. James FC (1970) Geographic size variation in birds and its relationship to climate. Ecology (3):365–390Google Scholar
  27. Jiang T, Metzner W, You Y, Liu S, Lu G, Li S, Wang L, Feng J (2010) Variation in the resting frequency of Rhinolophus pusillus in mainland China, effect of climate and implications for conservation. J Acoust Soc Am 128:2204–2221Google Scholar
  28. Jiang T, Wu H, Feng J (2015) Patterns and causes of geographic variation in bat echolocation pulses. Integr Zool 10:241–256Google Scholar
  29. Jones G (1996) Does echolocation constrain the evolution of body size in bats? In: Symposia of the Zoological Society of London, The Society, London, 1960–1999, pp 111–128Google Scholar
  30. Kalcounis MC, Brigham RM (1995) Intraspecific variation in wing loading affects habitat use by little brown bats (Myotis lucifugus). Can J Zool 73:89–95Google Scholar
  31. Kirschel ANG, Slabberkoorn H, Blumstein DT, Cohen RE, de Kort SR, Buermann W, Smith TB (2011) Testing alternative hypotheses for evolutionary diversification in an African songbird: rainforest refugia versus ecological gradients. Evolution 65:3162–3174Google Scholar
  32. Kleinbaum DG, Kupper LL, Muller KE (1988) Applied regression analysis and other multivariable methods, 2nd ed. PWS-KENT Publishing Company, BostonGoogle Scholar
  33. Knöornschild M, Jung K, Nagy M, Metz M, Kalko E (2012) Bat echolocation calls facilitate social communication. Proc R Soc B: Biol Sci 279(1748):4827e4835Google Scholar
  34. Kunz TH, Parsons S (2009) Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, BaltimoreGoogle Scholar
  35. Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334Google Scholar
  36. Lawrence BD, Simmons JA (1982) Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J Acoust Soc Am 71(3):585–590CrossRefPubMedGoogle Scholar
  37. Leinonen T, O’Hara, R, Cano J, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evolut Biol 21:1–17Google Scholar
  38. Luo J, Kosel K, Zsebok S, Siemers BM, Goerlitz HR (2014) Global warming alters sound transmission: differential impact on the prey detection ability of echolocating bats. J R Soc Interface/R Soc 11:20130961.  https://doi.org/10.1098/rsif.2013.0961PMID:24335559
  39. Malhotra A, Thorpe RS (2000) The dynamics of natural selection and vicariance in the dominican anole: patterns of within-island molecular and morphological divergence. Evolution 54:245–258Google Scholar
  40. Maluleke T, Jacobs DS, Winker H (2017) Environmental correlates of geographic divergence in a phenotypic trait: a case study using bat echolocation. Ecol Evolut 2017,00:1–15.  https://doi.org/10.1002/ece3.3251
  41. Marroig G, Cheverud JM (2004) Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? Am Nat 163:417–428Google Scholar
  42. Millstein RL (2002) Are random drift and natural selection conceptually distinct? Biol Philos 17:33–53Google Scholar
  43. Monadjem A, Taylo, PJ, Cotterill FPD, Schoeman CM (2010) Bats of southern and central Africa: a biogeographic and taxonomic synthesis. Wits University Press, JohannesburgGoogle Scholar
  44. Morrone JJ (2009) Evolutionary biology: an intergrative approach with case studies Columbia University Press, ColumbiaGoogle Scholar
  45. Moussy C, Hosken D, Mathews F, Smith G, Aegerter J, Bearhop S (2013) Migration and dispersal patterns of bats and their influence on genetic structure. Mamm Rev 43:183–195Google Scholar
  46. Mutumi GL, Jacobs DS, Winker H (2016) Sensory drive mediated by climatic gradients partially explains divergence in acoustic signals in two horseshoe bat species, Rhinolophus swinnyi and Rhinolophus simulator. Plos ONE 11:e0148053.  https://doi.org/10.1371/journal.pone.0148053
  47. Mutumi GL, Jacobs DS, Winker H (2017) The relative contribution of drift and selection to phenotypic divergence: a test case using the horseshoe bats Rhinolophus simulator and Rhinolophus swinnyi. Ecol Evolut 2017:1–14.  https://doi.org/10.1002/ece3.2966
  48. Neuweiler G (1984) Foraging, echolocation and audition in bats. Naturwissenschaften 71:446–455CrossRefGoogle Scholar
  49. Neuweiler G (1989) Foraging ecology and audition in echolocating bats. Trends Ecol Evol 4(6):160–166CrossRefPubMedGoogle Scholar
  50. Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc Lond B Biol Sci 316:335–427Google Scholar
  51. Odendaal LJ, Jacobs DS, Bishop JM (2014) Sensory trait variation in an echolocating bat suggests roles for both selection and plasticity. BMC Evolut Biol 14:60.  https://doi.org/10.1186/1471-2148-14-60
  52. Ohmer ME, Robertson JM, Zamudio KR (2009) Discordance in body size, colour pattern, and advertisement call across genetically distinct populations in a Neotropical anuran (Dendropsophus ebraccatus). Biol J Linnean Soc 97:298–313Google Scholar
  53. Orr M R, Smith TB (1998) Ecology and speciation. Trends Ecol Evolut 13:502–506Google Scholar
  54. Puechmaille SJ, Borissov IM, Zsebok S, Allegrini B, Hizem M, Kuenzel S, Schuchmann, M, Teeling, EC, Siemers BM (2014) Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi. Plos ONE 9(7):e103452.  https://doi.org/10.1371/journal.pone.0103452
  55. R Development Core Team (2013) R: a language and environment for statistical computing, 3.1 edn. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  56. Racey PA (1988) Reproductive assessment in bats. In: Kunz TH (ed) Ecological and behavioural methods for the study of bats. Smithsonian Institution Press, Washington DC, pp 31–45Google Scholar
  57. Rogell B, Eklund M, Thörngren H, Laurila A, Höglund J (2010) The effects of selection, drift and genetic variation on life-history trait divergence among insular populations of natterjack toad, Bufo calamita. Mol Ecol 19:2229–2240Google Scholar
  58. Rughetti M, Toffoli R (2014) Sex-specific seasonal change in body mass in two species of Vespertilionid bats. Acta Chiropterologica 16(1):149–155Google Scholar
  59. Schnitzler H-U, Denzinger A (2011) Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals. J Comp Physiol A: Neuroethol Sens Neural Behav Physiol 197(5):541–559Google Scholar
  60. Schnitzler H-U, Kalko EK (2001) Echolocation by insect-eating bats: we define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. BioScience 51:557–569Google Scholar
  61. Schuchmann M, Siemers B (2010) Behavioural evidence for community-wide species discrimination from echolocation calls in bats. Am Nat 176:72–82CrossRefPubMedGoogle Scholar
  62. Schuller G, Neuweiler G, Schnitzler H-U (1971) Collicular responses to the frequency modulated final part of echolocation sounds in Rhinolophus ferrrumequinum. Zeitschrift für vergleichende Physiologie 74:153–155Google Scholar
  63. Siemers BM, Beedholm K, Dietz C, Dietz I, Ivanova T (2005) Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica 7:259–274Google Scholar
  64. Smith HF (2011) The role of genetic drift in shaping modern human cranial evolution: a test using microevolutionary modeling. Int J Evolut Biol 2011 Article ID 145262, 11 pp.  https://doi.org/10.4061/2011/145262
  65. Stoffberg S, Jacobs DS, Matthee CA (2011) The divergence of echolocation frequency in horseshoe bats: moth hearing, body size or habitat? J Mamm Evolut 18:117–129.  https://doi.org/10.1007/s10914-011-9158-x
  66. Sun KP, Luo L, Kimball R, Weiet X, jin L, Jiang T, Li G, Feng J (2013) Geographic variation in the acoustic traits of greater horseshoe bats, testing the importance of drift and ecological selection in evolutionary processes. Plos ONE 8:e70368.  https://doi.org/10.1371/journal.pone.0070368
  67. Taylor PJ, Stoffberg S, Monadjem A, Schoeman MC, Bayliss J, Cotterill FPD (2012). Four new bat species (Rhinolophus hildebrandtii Complex) reflect Plio-Pleistocene divergence of dwarfs and giants across an Afromontane Archipelago. Plos ONE 7(9):e41744.  https://doi.org/10.1371/journal.pone.0041744
  68. Turelli M (1988) Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution 42:1342–1347Google Scholar
  69. von Cramon-Taubadel N (2013) Evolutionary insights into global patterns of human cranial diversity: population history, climatic and dietary effects. J Anthropol Sci 91:1e36Google Scholar
  70. Weaver TD, Roseman CC, Stringer CB (2007) Were neandertal and modern human cranial differences produced by natural selection or genetic drift? J Hum Evolut 53:135–145Google Scholar
  71. Whitlock MC (2000) Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54:1855–1861Google Scholar
  72. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedPubMedCentralGoogle Scholar
  73. Yoshino H, Matsumura S, Kinjo K, Tamura H, Ota H, Izawa M (2006) Geographical variation in echolocation call and body size of the Okinawan least horseshoe bat, Rhinolophus pumilus (Mammalia, Rhinolophidae), on Okinawa-jima Island, Ryukyu Archipelago, Japan. Zool Sci 23:661–667Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Cape TownCape TownSouth Africa
  2. 2.School of Natural SciencesUniversity of CaliforniaMercedUSA

Personalised recommendations