A Nuclear DNA Phylogenetic Perspective on the Evolution of Echolocation and Historical Biogeography of Extant Bats (Chiroptera)

Abstract

Bats (Order Chiroptera), the only mammals capable of powered flight and sophisticated laryngeal echolocation, represent one of the most species-rich and ubiquitous orders of mammals. However, phylogenetic relationships within this group are poorly resolved. A robust evolutionary tree of Chiroptera is essential for evaluating the phylogeny of echolocation within Chiroptera, as well as for understanding their biogeographical history. We generated 4 kb of sequence data from portions of four novel nuclear intron markers for multiple representatives of 17 of the 18 recognized extant bat families, as well as the putative bat family Miniopteridae. Three echolocation-call characters were examined by mapping them onto the combined topology: (1) high-duty cycle versus low-duty cycle, (2) high-intensity versus low-intensity call emission, and (3) oral versus nasal emission. Echolocation seems to be highly convergent, and the mapping of echolocation-call design onto our phylogeny does not appear to resolve the question of whether echolocation had a single or two origins. Fossil taxa may also provide insight into the evolution of bats; we therefore evaluate 195 morphological characters in light of our nuclear DNA phylogeny. All but 24 of the morphological characters were found to be homoplasious when mapped onto the supermatrix topology, while the remaining characters provided insufficient information to reconstruct the placement of the fossil bat taxa with respect to extant families. However, a morphological synapomorphy characterizing the Rhinolophoidea was identified and is suggestive of a separate origin of echolocation in this clade. Dispersal-Vicariance analysis together with a relaxed Bayesian clock were used to evaluate possible biogeographic scenarios that could account for the current distribution pattern of extant bat families. Africa was reconstructed as the center of origin of modern-day bat families.

The developmental basis of bat wing muscle

“…Therefore, the developmental programme that mobilizes adjacent muscular tissues for the precursors of the wing membranes might have been adopted in the initial phase of chiropteran evolution, in parallel with the acquisition of the wing itself. Furthermore, recent molecular phylogeny of extant bat species clearly identifies two major lineages within the order-suborders Yinpterochiroptera and Yangochiroptera 2,53,54 . In the present study, we revealed that the occipito-pollicalis of Miniopterus fuliginosus (family Miniopteridae), which is a member of Yangochiroptera, is solely innervated by cranial nerve VII.…”

Evolution of the placenta and associated reproductive characters in bats

“…These were then mapped on a pre-existing hypothesis of bat relationships. We used a tree (Miller-Butterworth et al, 2007) that is in broad agreement with two other major studies in molecular phylogenetics (Eick et al, 2005;Teeling et al, 2005). Our purpose was threefold.…”

“…First, recent advances in molecular phylogenetics indicate that the order Chiroptera is monophyletic, putting to rest the idea of separate origins for the echolocating microbats and the nonecholocating, frugivorous megabats (Murphy et al, 2001;Eick et al, 2005;Teeling et al, 2005;MillerButterworth et al, 2007). Even evidence from other systems is overwhelmingly in support of bats as a monophyletic clade (Simmons, '94;Jones et al, 2002), although proponents of a separate Published online 14 May 2008 in Wiley InterScience (www.…”

“…There is general agreement to recognize four superfamilies of microbats (Smith, '76;Eick et al, 2005;Teeling et al, 2005;Miller-Butterworth et al, 2007). These are currently (1) Rhinolophoidea (Rhinolophidae, Megadermatidae, Craseonycteridae, Rhinopomatidae); (2) Emballonuroidea (Emballonuridae, Nycteridae); (3) Noctilionoidea (Phyllostomidae, Mormoopidae, Noctilionidae, Furipteridae, Thyropteridae, Mystacinidae, Myzopodidae); and (4) Vespertilionoidea (Vespertilionidae, Molossidae, Miniopteridae, Natalidae).…”

“…These are currently (1) Rhinolophoidea (Rhinolophidae, Megadermatidae, Craseonycteridae, Rhinopomatidae); (2) Emballonuroidea (Emballonuridae, Nycteridae); (3) Noctilionoidea (Phyllostomidae, Mormoopidae, Noctilionidae, Furipteridae, Thyropteridae, Mystacinidae, Myzopodidae); and (4) Vespertilionoidea (Vespertilionidae, Molossidae, Miniopteridae, Natalidae). The recent molecular studies find that Rhinolophoidea shares a common ancestor with the megabats as Pteropodiformes (Eick et al, 2005) or Yinpterochiroptera (Teeling et al, 2005). This hypothesis is controversial as it has profound implications for the evolution of echolocation (Jones and Teeling, 2006).…”