The evolution of echolocation in bats

https://doi.org/10.1016/j.tree.2006.01.001Get rights and content

Recent molecular phylogenies have changed our perspective on the evolution of echolocation in bats. These phylogenies suggest that certain bats with sophisticated echolocation (e.g. horseshoe bats) share a common ancestry with non-echolocating bats (e.g. Old World fruit bats). One interpretation of these trees presumes that laryngeal echolocation (calls produced in the larynx) probably evolved in the ancestor of all extant bats. Echolocation might have subsequently been lost in Old World fruit bats, only to evolve secondarily (by tongue clicking) in this family. Remarkable acoustic features such as Doppler shift compensation, whispering echolocation and nasal emission of sound each show multiple convergent origins in bats. The extensive adaptive radiation in echolocation call design is shaped largely by ecology, showing how perceptual challenges imposed by the environment can often override phylogenetic constraints.

Section snippets

Echolocation and the diversity of bats

Bats are perhaps the most unusual and specialized of all mammals. Together with birds, they are the only extant vertebrates that are capable of powered flight. Bats have mastered the night skies largely by using echolocation (biosonar) to perceive their surroundings 1, 2. Indeed flight and echolocation are largely responsible for the global success, species richness and the ability of bats to exploit diverse niches (see Online Supplementary Material). How, when and why did bats evolve these

The position of bats in the mammalian phylogenetic tree

Questions concerning the evolutionary origin of bats have long intrigued biologists and resulted in many phylogenetic studies, the results of which have caused heated and lengthy debates 3, 4, 5, 6. The position of bats within Mammalia and the monophyly of the order itself were questions that dominated the 1980s and 1990s. Currently, there is overwhelming molecular and morphological evidence to support the monophyly of bats and, thus, a single origin of flight in mammals 7, 8, 9, 10. Recent

Morphological consensus

Before the dawn of molecular studies, bat systematics was dominated by palaeontological and morphological data. The most prominent morphological tree in the literature during the 1970s and 1980s was derived from the classification system of Miller [18] and was proposed by Smith [19] and Van Valen [20]. This tree was later modified by Koopman [21] and has been supported mainly by both large morphological datasets 17, 22 and supertree consensus studies [23]. The first major division in this tree

Emerging molecular consensus

The major structure of the bat phylogenetic tree based on molecular data (i.e. microbat paraphyly) was apparent with the first molecular phylogenetic studies. Based on transferrin immunological distance data, microbats were found to be paraphyletic; however, this result was initially reported as an artifact because it was so unexpected (E.D. Pierson, PhD dissertation, University of California, Berkeley, 1986). Whole genome DNA–DNA hybridization studies also supported the association of

Adaptive radiation and convergent evolution of echolocation calls in extant bats

One recent attempt to categorize bat echolocation calls considered three major types of echolocation call: broadband, narrowband and long constant frequency (CF) with Doppler-shift compensation (DSC) [35]. Other than differing in the pattern of frequency structure over time, bat signals also vary in their intensity and harmonic composition. Sophisticated methods for reconstructing bat flight tracks in three-dimensions 36, 37 have enabled the accurate localization of flying bats in relation to

Mapping call structure onto phylogeny highlights the presence of convergence

Attempts to map echolocation call structure onto phylogeny can be informative and have shown, for example, that the single clicks used by cave swiftlets have evolved from double clicks at least twice [64]. However, the large variation in call diversity within and between bat families renders the evolutionary reconstruction of signal types unclear (Figure 1). Overall, our perspective on the evolution of echolocation is clouded by the diversity and plasticity of signals that we see in extant

Conclusions and future directions

It is important that echolocation calls are recorded from some little studied species (e.g. those in Furipteridae, Thyropteridae and Natalidae) to complete our understanding of call diversity in bats. Recording the low-intensity echolocation calls produced by many of these bats in nature remains a challenge. Field studies are essential because familiarity with surroundings might influence how the bat uses echolocation under laboratory conditions [67]. Clearly, many of the diverse echolocation

Acknowledgements

We thank Brock Fenton and two anonymous referees for comments on the article.

References (73)

  • E.C. Teeling

    A molecular phylogeny for bats illuminates biogeography and the fossil record

    Science

    (2005)
  • R.M. Adkins et al.

    Molecular phylogeny of the superorder Archonta

    Proc. Natl. Acad. Sci. U. S. A.

    (1991)
  • W.J. Bailey

    Rejection of the “flying primate” hypothesis by phylogenetic evidence from the ε-globin gene

    Science

    (1992)
  • E.C. Teeling

    Molecular evidence regarding the origin of echolocation and flight in bats

    Nature

    (2000)
  • O. Madsen

    Parallel adaptive radiations in two major clades of placental mammals

    Nature

    (2001)
  • W.J. Murphy

    Molecular phylogenetics and the origins of placental mammals

    Nature

    (2001)
  • W.J. Murphy

    Resolution of the early placental mammal radiation using Bayesian phylogenetics

    Science

    (2001)
  • D.E. Pumo

    Complete mitochondrial genome of a Neotropical fruit bat, Artibeus jamaicensis, and a new hypothesis of relationships of bats to other eutherian mammals

    J. Mol. Evol.

    (1998)
  • M.J. Novacek

    Mammalian phylogeny: shaking the tree

    Nature

    (1992)
  • N.B. Simmons et al.

    Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera

    Bull. Am. Mus. Nat. Hist.

    (1998)
  • G. Miller

    The families and genera of bats

    U.S. Natl. Mus. Bull.

    (1907)
  • Smith, J.D. (1976) Chiropteran evolution. In Biology of Bats of the New World Family Phyllostomatidae (Part I) (Baker,...
  • L. Van Valen

    The evolution of bats

    Evol. Theory

    (1979)
  • K.F. Koopman

    Chiroptera: Systematics. Part 60. Handbook of Zoology. Vol. 8

    (1994)
  • G.F. Gunnel et al.

    Fossil evidence and the origin of bats

    J. Mamm. Evol

    (2005)
  • K.E. Jones

    A phylogenetic supertree of the bats (Mammalia: Chiroptera)

    Biol. Rev.

    (2002)
  • M.S. Springer

    Integrated fossil and molecular data reconstruct bat echolocation

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • E.C. Teeling

    Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid bats

    Proc. Natl. Acad. Sci. U. S. A.

    (2002)
  • R.A. Van Den Bussche et al.

    Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxa

    J. Mamm.

    (2004)
  • G.N. Eick

    A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera)

    Mol. Biol. Evol.

    (2005)
  • J.M. Hutcheon et al.

    Camping in a different tree: results of molecular systematic studies of bats using DNA–DNA hybridization

    J. Mamm. Evol.

    (2004)
  • J.M. Hutcheon

    Base-compositional biases and the bat problem. III. The question of microchiropteran monophyly

    Philos. Trans. R. Soc. London Ser. B

    (1998)
  • R.J. Baker

    DNA synapomorphies for a variety of taxonomic levels from a cosmid library from the New World bat Macrotus waterhousii

    Syst. Biol.

    (1997)
  • F-G.R. Liu et al.

    A phylogenetic assessment of molecular and morphological data for eutherian mammals

    Syst. Biol.

    (1999)
  • P. Hulva et al.

    Craseonycteris thonglongyai (Chiroptera: Craseonycteridae) is a rhinolophoid: molecular evidence from cytochrome b

    Acta Chiropterol.

    (2002)
  • M. Volleth

    A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families

    Chromosome Res.

    (2002)
  • Cited by (0)

    View full text