Evolution and systematics of the Aculeata and kin (Hymenoptera), with emphasis on the ants (Formicoidea: †@@@idae fam. nov., Formicidae)

Abstract

Fossils not only provide unique opportunity to understand the "tempo and mode" of evolution but are essential for modeling lineage-contingent diversification histories. Here, we interrogate the Mesozoic fossil record of the Aculeata, with emphasis on the ants (Formicidae), and conduct an extended series of ancestral state estimation exercises on distributions of tip-dated combined-evidence phylogenies. We developed and illustrated from ground-up a set of 576 morphological characters which we scored for 144 extant and 431 fossil taxa; we used average posterior probability support to filter this to a target matrix of 303 taxa, for which we integrated strongly filtered ultraconserved element (UCE) data for 115 living species. We also implemented reversible jump MCMC (rjMCMC) and hidden state methods to model complex behavioral characters to test hypotheses about the pathway to obligate eusociality. In addition to revising the higher classification of all sampled groups to family or subfamily level using estimated character polarities to diagnose nodes across the phylogeny, we find that the mid-Cretaceous genera †Camelomecia and †Camelosphecia form a clade which is robustly supported as sister to the total clade Formicidae. For this reason, we name this extinct clade as †@@@idae fam. nov. and provide a definition for the expanded Formicoidea. Based on our results, we recognize three major phases in the early evolution of the ants: (1) origin of ants as running-adapted huntresses during the Late Jurassic in the "stinging aggressor" guild (Aculeata) among various lineages of "sneaking parasitoids" (non-aculeate Vespina); (2) the first formicoid radiation during the Early Cretaceous, by the end of which all major extant ant linages had originated; and (3) turnover of the Formicoidea at the end-Cretaceous leading to the second formicoid radiation, i.e., the Cenozoic formicid diversification. We conclude with a concentrated series of considerations for future directions of study with this dataset and beyond.

Ant phylogenomics reveals a natural selection hotspot preceding the origin of complex eusociality

“…This suggests the possibility that subterranean lifestyles existed in the ancestors of extant ants or, more likely, that a hypogeic lifestyle originated at an early stage in the history of leptanillomorphs. This result contrasts with the fossil evidence, because the earliest-known fossilized crown ants were not specialized to subterranean habitats and come from Burmese amber deposits that are approximately 99 million years old 15,16 . Set against our divergence date estimates, this indicates a gap in the ant fossil record of ~50 million years, further emphasizing an existing discrepancy between fossils and molecular data when it comes to the question of ant origins 17 .…”

“…Similarly, it is possible that the abundance of crown ants was low at first, and only sufficiently increased with the rise of angiosperm 6 to be represented in the fossil record. Alternatively, there may be methodological biases leading to overestimation of divergence dates 20,21 or incorrect phylogenetic placement of early ant fossils 16 .…”

The ant abdomen: The skeletomuscular and soft tissue anatomy of Amblyopone australis workers (Hymenoptera: Formicidae)

“…It must be noted that the supposedly “basal” position of the Amblyoponinae within Formicidae has led to inaccurate inferences about the evolutionary context of skeletomuscular characters in the past. For example, the broad attachment of AII to AIII is a derived condition in amblyoponines (Bolton, 2003; Boudinot et al, 2020, 2022b), not a symplesiomorphy with outgroup aculeates (Hashimoto, 1996; Wilson et al, 1967). We therefore encourage caution in interpreting characters as plesiomorphies due to an assumed “primitive” phylogenetic position, and especially of the amblyoponine plan as paradigmatic of the ancestral ant sting (Kugler, 1978).…”

“…In ants, the anterior metasomal segments have undergone further characteristic modification: in addition to the apocritan constriction between mesosoma and metasoma (the “wasp waist”), another constriction occurs between at least metasomal segments I and II, and between metasomal segments II and III in some lineages (the “ant waist” or petiole and postpetiole; Bolton, 2003; Gauld & Bolton, 1988). Other apomorphies of the anterior metasoma include the gain of a subpetiolar process and the prora of the third abdominal segment (Boudinot et al, 2020, 2022b). The flexibility and maneuverability of the metasoma is facilitated by the anterior abdominal skeletomusculature and has important consequences for the functions of the terminal abdominal segments, including the sting in females and genital capsule in males.…”

“…The sting itself is an evolutionarily plastic organ, derived from the ovipositor, which has acquired diverse functions including prey paralysis, defense against predators and competitors, and dissemination of pheromones, and which is reduced or absent in various lineages (Hölldobler & Wilson, 1990; Oeser, 1961). The “vespiform” Aculeata, that is, all aculeates to the exclusion of the traditional chrysidoid families, are defined in part by complete internalization of abdominal tergum VIII in females (Boudinot et al, 2022b; Brothers, 1975; Brothers & Carpenter, 1993; Carpenter, 1986; Oeser, 1961; Rasnitsyn, 1988; Ronquist et al, 1999). Examples of derived abdominal functions in ants include mechanical attachment in social carrying (Möglich & Hölldobler, 1974) and self‐assembled structures during nest construction (Hölldobler & Wilson, 1990) and predation (Peeters & De Greef, 2015); “reversed” phragmosis, that is, nest entrance plugging with the gaster (Brown, 1967; Poldi, 1963); and prey manipulation (Masuko, 2020).…”