Morphological and Molecular Insights into Aleocharine Rove Beetle Evolution

Abstract

Aleocharinae is the largest subfamily in the largest family of beetles, the rove beetles. The subfamily has at least 61,575 species divided into 63 tribes, and is arguably one of the most taxonomically and ecologically diverse lineage of extant metazoans. Among the Aleocharinae, 99% of the taxonomic diversity and ecological diversity belongs to a lineage characterized by the presence of a tergal gland, the gland-clade, which ancestrally functions as a defensive weapon. Subsequent reprogramming of glandular chemistry has taken place, particularly in lineages that have evolved to live with social insects, or ants and termites in particular. In addition, many of these symbiotic groups have evolved additional glands throughout their bodies, demonstrating the inherently adaptive nature of glands in the aleocharine body plan. Therefore, it is possible that the tergal gland was a key innovation that fueled aleocharine diversification. However, very little is known about the early evolution of no-gland lineages, in particular, what anatomical changes may have accompanied the evolutionary origin of the tergal gland. Molecular phylogenetic analyses of the tachyporine-group and early diverging Aleocharinae were conducted. The tachyporine-group was not recovered as a monophyletic group. While Habrocerinae, Olisthaerinae, Phloeocharinae, and Trichophyinae were recovered forming a clade, Aleocharinae and Tachyporinae nested outside of this group. Tachyporinae was recovered polyphyletic and Tachyporini sister to Aleocharinae, supported by the shared presence of a hind coxal lamella. Aleocharinae was recovered monophyletic with no-gland tribes forming an early diverging grade leading up to a monophyletic gland-clade. The unique multisegmented paramere is the most characteristic and an unambiguous synapomorphy for Aleocharinae. The gland-clade was recovered non-monophyletic due to the exclusion of Hypocyphtini, potentially implying an independent evolution of the tergal gland in this tribe. The long presumed sister-group relationship between Gymnusini and Deinopsini was not recovered, despite many shared anatomical similarities. Although similarities between Deinopsini and Gymnusini may be the result of convergence, I hypothesize that their overall anatomy is plesiomorphic for the subfamily. I further hypothesize that the tergal gland acting as a key innovation was contingent on the abandonment of the ancestrally limuloid bodyform at the common ancestor of the gland- clade, and combined with increased sexual selection, fueled gland-clade diversification. The morphology of Aleocharinae was reevaluated in light of the results obtained from phylogenetic analyses of the tachyporine-group and no-gland aleocharine tribes. A total of 328 anatomical terms are recognized in this study, with 77 or 23% being novel. Plotting number of terms by character system revealed that the majority of the variation belongs to the mouthparts (52%), followed by a far second male genitalia (19%). Based on the distribution of anatomical terms, it is likely that the majority of morphological phylogenetic characters for Aleocharinae will stem from mouthparts variation. The reevaluated Aleocharinae morphology was tested in a phylogenetic context using the Hoplandriini as a case study, and as predicted, the majority of characters in the dataset were mouthparts in origin; this pattern is probably generalizable across Aleocharinae. The dataset performed well at the intratribal level, but overall lacked moderately slowly evolving characters, which may be reflected in the lack of resolution at the intertribal level. Larval characters were found to be generally slower evolving, and pending further knowledge of their anatomy, may be a useful source for additional characters for phylogeny reconstruction.