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Interrogating Phylogenetic Discordance Resolves Deep Splits in the Rapid Radiation of Old World Fruit Bats (Chiroptera: Pteropodidae).

ABSTRACT: The family Pteropodidae (Old World fruit bats) comprises $>$200 species distributed across the Old World tropics and subtropics. Most pteropodids feed on fruit, suggesting an early origin of frugivory, although several lineages have shifted to nectar-based diets. Pteropodids are of exceptional conservation concern with $>$50% of species considered threatened, yet the systematics of this group has long been debated, with uncertainty surrounding early splits attributed to an ancient rapid diversification. Resolving the relationships among the main pteropodid lineages is essential if we are to fully understand their evolutionary distinctiveness, and the extent to which these bats have transitioned to nectar-feeding. Here we generated orthologous sequences for $>$1400 nuclear protein-coding genes (2.8 million base pairs) across 114 species from 43 genera of Old World fruit bats (57% and 96% of extant species- and genus-level diversity, respectively), and combined phylogenomic inference with filtering by information content to resolve systematic relationships among the major lineages. Concatenation and coalescent-based methods recovered three distinct backbone topologies that were not able to be reconciled by filtering via phylogenetic information content. Concordance analysis and gene genealogy interrogation show that one topology is consistently the best supported, and that observed phylogenetic conflicts arise from both gene tree error and deep incomplete lineage sorting. In addition to resolving long-standing inconsistencies in the reported relationships among major lineages, we show that Old World fruit bats have likely undergone at least seven independent dietary transitions from frugivory to nectarivory. Finally, we use this phylogeny to identify and describe one new genus. [Chiroptera; coalescence; concordance; incomplete lineage sorting; nectar feeder; species tree; target enrichment.].

SUBMITTER: Nesi N

PROVIDER: S-EPMC8513763 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe 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.ResultsOur 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.ConclusionsThe 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.

Project description:We examined patterns of genetic variation in Rousettus madagascariensis from Madagascar and R. obliviosus from the Comoros (Grande Comore, Anjouan, and Mohéli). Genetic distances among individuals on the basis of 1,130 base pairs of the mitochondrial cytochrome b (Cytb) locus were estimated from specimens collected from 17 sites on Madagascar, 3 sites on Grande Comore, 3 sites on Anjouan, and 2 sites on Mohéli. We observed little variation in Madagascar and nearshore island samples (maximum 1.1%) and interisland Comoros samples (maximum 1.8%). In contrast, pairwise distances between different sampled sites on Madagascar and the Comoros varied from 8.5% to 13.2%. For 131 Malagasy animals, 69 unique haplotypes were recovered with 86 variable sites, and for 44 Comorian individuals, 17 unique haplotypes were found with 30 variable sites. No haplotype was shared between Madagascar and the Comoros, adding to previous morphological evidence that these 2 populations should be considered separate species. Cytb data showed that Rousettus populations of Madagascar (including nearshore islands) and the Comoros are respectively monophyletic and display no geographic structure in haplotype diversity, and that R. madagascariensis and R. obliviosus are strongly supported as sister to each other relative to other Rousettus species. Genotypic data from 6 microsatellite loci confirm lack of geographic structure in either of the 2 species. In pairwise tests of population differentiation, the only significant values were between samples from the Comoro Islands and Madagascar (including nearshore islands). Estimates of current and historical demographic parameters support population expansion in both the Comoros and Madagascar. These data suggest a more recent and rapid demographic expansion in Madagascar in comparison with greater population stability on the Comoros. On the basis of available evidence, open-water crossings approaching 300 km seem rarely traversed by Rousettus, and, if successful, can result in genetic isolation and subsequent differentiation.

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Interrogating Phylogenetic Discordance Resolves Deep Splits in the Rapid Radiation of Old World Fruit Bats (Chiroptera: Pteropodidae).

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