Phylogenomic Analyses Elucidate the Evolutionary Relationships of Bats

Abstract

Molecular phylogenetics has rapidly established the evolutionary positions of most major mammal groups, yet analyses have repeatedly failed to agree on that of bats (order Chiroptera). Moreover, the relationship among the major bat lineages has proven equally contentious, with ongoing disagreements about whether echolocating bats are paraphyletic or a true group having profound implications for whether echolocation evolved once or possibly multiple times. By generating new bat genome data and applying model-based phylogenomic analyses designed to accommodate heterogeneous evolutionary processes, we show that-contrary to recent suggestions-bats are not closely related to odd-toed ungulates but instead have a more ancient origin as sister group to a large clade of carnivores, ungulates, and cetaceans. Additionally, we provide the first genome-scale support showing that laryngeal echolocating bats are not a true group and that this paraphyly is robust to their position within mammals. We suggest that earlier disagreements in the literature may reflect model misspecification, long-branch artifacts, poor taxonomic coverage, and differences in the phylogenetic markers used. These findings are a timely reminder of the relevance of experimental design and careful statistical analysis as we move into the phylogenomic era.

Nonecholocating Fruit Bats Produce Biosonar Clicks with Their Wings

“…Echolocation, the ability to perceive the world acoustically by emitting sound pulses and analyzing the returning echoes, has evolved in at least three different animal groups (birds [13], cetaceans [14,15], and bats [16]), and possibly also other mammals such as in shrews [17] and tenrecs [18] (see Table 1). There is an ongoing debate as to whether bat echolocation evolved once or twice [4][5][6][7][8][9][10]. It is, however, agreed that more than 1,200 bat species [21] can be divided into w85% echolocating species and w15% Old World fruit bats (family Pteropodidae) that are currently classified as nonecholocating [3,[10][11][12], with the exception of a few species in the genus Rousettus that use lingual echolocation [22,23].…”

“…There is an ongoing debate as to whether bat echolocation evolved once or twice [4][5][6][7][8][9][10]. Bats of the genus Rousettus evolved their lingual echolocation independently according to both hypotheses.…”

“…Accordingly, there is an ongoing debate regarding the evolution of bat echolocation [4][5][6][7][8][9][10]. In search of the origin of bat echolocation, we studied how Old World fruit bats, which have always been classified as nonecholocating [3,[10][11][12], orient in complete darkness. We found that two of these nonecholocating species used click-like sounds to detect and discriminate objects in complete darkness.…”

“…There is an ongoing debate as to whether bat echolocation evolved once or twice [4][5][6][7][8][9][10]. It is, however, agreed that more than 1,200 bat species [21] can be divided into w85% echolocating species and w15% Old World fruit bats (family Pteropodidae) that are currently classified as nonecholocating [3,[10][11][12], with the exception of a few species in the genus Rousettus that use lingual echolocation [22,23]. Being nocturnal mammals, ''nonecholocating'' Old World fruit bats often fly at very low light levels.…”

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species

“…Molecular phylogenetic analyses have reclassified their position within the mammalian tree (25)(26)(27), refuting their position within Archonta (including Primates, Scandentia, and Dermoptera) and placing them within Laurasiatheria (including Carnivora, Perissodactyla, Eulipotyphla, Pholidota, and Cetartiodactyla); and reclassified familial and interordinal relationships (Figure 1) (5,23). Despite these advances, however, the sister taxon to bats remains unresolved (for review, see 23).…”