Phylogenomic insights into the worldwide evolutionary relationships of the stingless bees (Apidae, Meliponini)

Abstract

Stingless bees (tribe Meliponini) are remarkable for their characteristically large social colonies, their capacity to produce honey and other useful products, and their morphological and behavioral diversity. They have a disjunct pan-tropical distribution, primarily occurring in warm and humid environments in the Neotropical, Afrotropical, and Indo-Australasian regions. Even though phylogenetic hypotheses have been proposed for Meliponini based on morphology and molecular data, many questions are still unsolved regarding the evolutionary relationships and systematics of the tribe. In this contribution, we present a large phylogenomic dataset comprising over 2500 ultra-conserved element (UCE) loci sequenced for 153 species of Meliponini, representing all known genera of stingless bees. The genera Camargoia, Paratrigonoides, Plectoplebeia, Cleptotrigona, Ebaiotrigona, Papuatrigona, Pariotrigona, Platytrigona, and Sahulotrigona were included in molecular phylogenetic analyses for the first time. Concatenated and species-tree analyses were performed using different partitioning strategies and summary methods. We performed gene-genealogy interrogation (GGI) on several recalcitrant nodes to resolve discordances among recovered tree topologies. Results were mostly consistent among analyses, recovering three main lineages of Meliponini congruent with the biogeographic domains to which they are associated. Within major clades, discordances were found in relation to previous works. The genus Frieseomelitta was recovered as paraphyletic in relation to Trichotrigona, and the genus Lepidotrigona was revealed to be composed of two independent lineages. Even though concatenated and weighted ASTRAL analyses were mostly effective in recovering the relationships favored by GGI, they retrieved different results in relation to the phylogenetic placements of Oxytrigona and Cephalotrigona. The most favored hypothesis in GGI analyses was not found in any other analyses, being more congruent with morphological evidence and highlighting the relevance of exploring the support given to alternative hypotheses through topological tests. Recent advances in our capacity to generate molecular sequences from old specimens using modern sequencing methods allowed for unparalleled sampling across genera, yielding a backbone for the phylogenetic relationships of stingless bees, which will further investigations into their systematics and evolution.