Evolutionary relationships of the old world fruit bats (Chiroptera, Pteropodidae): another star phylogeny?

Abstract

Background: The family Pteropodidae comprises bats commonly known as megabats or Old World fruit bats. Molecular phylogenetic studies of pteropodids have provided considerable insight into intrafamilial relationships, but these studies have included only a fraction of the extant diversity (a maximum of 26 out of the 46 currently recognized genera) and have failed to resolve deep relationships among internal clades. Here we readdress the systematics of pteropodids by applying a strategy to try to resolve ancient relationships within Pteropodidae, while providing further insight into subgroup membership, by 1) increasing the taxonomic sample to 42 genera; 2) increasing the number of characters (to >8,000 bp) and nuclear genomic representation; 3) minimizing missing data; 4) controlling for sequence bias; and 5) using appropriate data partitioning and models of sequence evolution.

Results: Our analyses recovered six principal clades and one additional independent lineage (consisting of a single genus) within Pteropodidae. Reciprocal monophyly of these groups was highly supported and generally congruent among the different methods and datasets used. Likewise, most relationships within these principal clades were well resolved and statistically supported. Relationships among the 7 principal groups, however, were poorly supported in all analyses. This result could not be explained by any detectable systematic bias in the data or incongruence among loci. The SOWH test confirmed that basal branches' lengths were not different from zero, which points to closely-spaced cladogenesis as the most likely explanation for the poor resolution of the deep pteropodid relationships. Simulations suggest that an increase in the amount of sequence data is likely to solve this problem.

Conclusions: The phylogenetic hypothesis generated here provides a robust framework for a revised cladistic classification of Pteropodidae into subfamilies and tribes and will greatly contribute to the understanding of character evolution and biogeography of pteropodids. The inability of our data to resolve the deepest relationships of the major pteropodid lineages suggests an explosive diversification soon after origin of the crown pteropodids. Several characteristics of pteropodids are consistent with this conclusion, including high species diversity, great morphological diversity, and presence of key innovations in relation to their sister group.

Figure 1

Single most parsimonious tree recovered with dataset 1. Tree scores are shown in Table 2. Numbers above branches are Bremer decay values and below branches are bootstrap percentages (when above 50%) obtained with 1000 replicates.

Figure 2

Maximum likelihood tree obtained with dataset 1 and partition scheme 6. Substitution models and parameters used are listed in the Additional file 6. Bootstrap values above 50% are shown next to branches.

Figure 3

P value of SH test versus length of simulated datasets. SH tests were done between ML best trees and derived trees with a collapsed node for the original dataset (8174 bp) and three simulated datasets (10 kb, 12 kb, and 14 kb). The simulated datasets were obtained with the same nucleotide frequency and substitution parameters found in the original dataset. Nodes A, B, C, D, and E are labeled in Figure 2.

Figure 4

Consensus of six most parsimonious trees obtained with dataset 2. Numbers shown above branches refer to Bremer decay values (left) and bootstrap percentages (right).

Figure 5

ML tree obtained with dataset 2 and partition scheme 6. Terminals in bold letters were represented in the data matrix by only two gene partitions. Bootstrap values greater than 50% are shown. Letters inside rectangles represent the inferred possible ancestral areas (labeled on the map insert and in the Additional file 9) for the referred clades.