Interrogating discordance resolves relationships in the rapid radiation of Old World fruit bats (Chiroptera: Pteropodidae)

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 shows 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.

狐蝠科（Pteropodidae，旧大陆果蝠）包含200余种物种，广泛分布于旧大陆的热带与亚热带区域。多数狐蝠以果实为食，这提示食果性（frugivory）的起源较早，尽管已有多个演化支转向以花蜜为食的食谱。狐蝠科的保护现状备受关注，超过50%的物种被列为受威胁物种，但该类群的分类系统学长期存在争议，其早期分化的不确定性被归因于一次古老的快速辐射演化。若要全面理解狐蝠科的演化独特性，以及这些蝙蝠转向食花蜜习性的程度，厘清其主要演化支间的系统发育关系至关重要。本研究针对114种旧大陆果蝠（隶属于43个属，分别覆盖现存物种与属级多样性的57%与96%）的1400余个核蛋白编码基因（nuclear protein-coding genes，共计280万个碱基对（base-pairs））构建了直系同源序列（orthologous sequences），并结合系统发育组学推断（phylogenomic inference）与信息含量过滤，以解析主要类群间的系统发育关系。串联法（concatenation）与基于溯祖理论的方法（coalescent-based methods）得到了三种不同的主干拓扑结构，无法通过系统发育信息含量过滤来调和。一致性分析与基因谱系溯源结果显示，其中一种拓扑结构始终得到最高支持度，而观测到的系统发育冲突同时源于基因树误差（gene tree error）与深度不完全谱系分选（deep incomplete lineage sorting）。除解决了长期以来关于主要类群间系统发育关系的争议之外，本研究还发现旧大陆果蝠可能至少经历了7次从食果性到食花蜜性（nectarivory）的独立饮食习性转变。最后，本研究利用该系统发育树鉴定并描述了一个新属。