Hox-logic of preadaptations for social insect symbiosis in rove beetles

How symbiotic lifestyles evolve from free-living ecologies is poorly understood. Novel traits mediating symbioses may stem from preadaptations: features of free-living ancestors that predispose taxa to engage in nascent interspecies relationships. In Metazoa's largest family, Staphylinidae (rove beetles), the body plan within the subfamily Aleocharinae is preadaptive for symbioses with social insects. Short elytra expose a pliable abdomen that bears targetable glands for host manipulation or chemical defense. The exposed abdomen has also been convergently refashioned into ant- and termite-mimicking shapes in multiple symbiotic lineages. Here we show how this preadaptive anatomy evolved via novel Hox gene functions that remodeled the ancestral coleopteran groundplan. Using the model staphylinid Dalotia coriaria, we abolished activities of the five thoracic and abdominal Hox genes. We show that elytral shortening is a staphylinid-specific property of the Hox-less appendage ground state, which is overridden in the metathorax by Ultrabithorax to promote hind wing expansion. In the exposed abdomen, we present evidence that defensive gland development stems from novel combinatorial outputs of the Abdominal-A and Abdominal-B Hox proteins: in the posterior compartment of tergite VI they specify a chemical gland reservoir, an imaginal disc-like invagination of ectodermal secretory cells; in the anterior compartment of tergite VII Abdominal-A and Abdominal-B specify clusters of classical duct-bearing glands. These distinct gland cell types collectively synthesize a blend of benzoquinone irritants, surfactant esters and alkane solvent, a defensive chemistry, which in symbiotic species has been augmented with specialized volatiles that potently manipulate ant behavior. These results reveal how Hox-controlled body axis modifications caused a convergent trend towards evolving symbiosis in the Metazoa

Hox-logic of body plan innovations for social symbiosis in rove beetles

How symbiotic lifestyles evolve from free-living ecologies is poorly understood. In Metazoa's largest family, Staphylinidae (rove beetles), numerous lineages have evolved obligate behavioral symbioses with ants or termites. Widespread convergence of this lifestyle is thought to stem from a novel, chemically defended body plan that enables free-living species to infiltrate colonies and undergo extreme evolutionary specialization. Here we show how this innovative body plan evolved, via new Hox functions in staphylinids that remodeled the coleopteran groundplan. Using a model staphylinid, Dalotia coriaria, we reveal the Hox basis for changes in thoracic appendage morphology that shortened the beetle elytron and left the abdomen physically unprotected, selecting for an abdominal defense gland that was likely key to unlocking ant and termite societies. We present evidence that the gland evolved through a novel, combinatorial role of the abdominal Hox proteins AbdA and AbdB. These proteins function together to specify distinct gland cell types in neighboring segmental compartments, each cell type synthesizing a different class of compound - irritant, ester and solvent. Only when secreted together do these compounds constitute a bioactive secretion, providing an example of emergent chemical functionality that arises from synergy between individual gland cell types. Hox-controlled specification of glandular diversity implies a modularity in compound biosynthesis that likely catalyzed the evolvability of rove beetle chemistry, including the capacity of symbiotic taxa to produce potent compounds for host deception. This study reveals how Hox-controlled body axis modifications predispose a major animal to convergently evolve into symbionts

Hox-logic of preadaptations for social insect symbiosis in rove beetles

How symbiotic lifestyles evolve from free-living ecologies is poorly understood. Novel traits mediating symbioses may stem from preadaptations: features of free-living ancestors that predispose taxa to engage in nascent interspecies relationships. In Metazoa's largest family, Staphylinidae (rove beetles), the body plan within the subfamily Aleocharinae is preadaptive for symbioses with social insects. Short elytra expose a pliable abdomen that bears targetable glands for host manipulation or chemical defense. The exposed abdomen has also been convergently refashioned into ant- and termite-mimicking shapes in multiple symbiotic lineages. Here we show how this preadaptive anatomy evolved via novel Hox gene functions that remodeled the ancestral coleopteran groundplan. Using the model staphylinid Dalotia coriaria, we abolished activities of the five thoracic and abdominal Hox genes. We show that elytral shortening is a staphylinid-specific property of the Hox-less appendage ground state, which is overridden in the metathorax by Ultrabithorax to promote hind wing expansion. In the exposed abdomen, we present evidence that defensive gland development stems from novel combinatorial outputs of the Abdominal-A and Abdominal-B Hox proteins: in the posterior compartment of tergite VI they specify a chemical gland reservoir, an imaginal disc-like invagination of ectodermal secretory cells; in the anterior compartment of tergite VII Abdominal-A and Abdominal-B specify clusters of classical duct-bearing glands. These distinct gland cell types collectively synthesize a blend of benzoquinone irritants, surfactant esters and alkane solvent, a defensive chemistry, which in symbiotic species has been augmented with specialized volatiles that potently manipulate ant behavior. These results reveal how Hox-controlled body axis modifications caused a convergent trend towards evolving symbiosis in the Metazoa

A new myrmecophilous genus of Falagriini from Colorado, USA (Coleoptera: Staphylinidae: Aleocharinae)

Eldredge, K. Taro (2022): A new myrmecophilous genus of Falagriini from Colorado, USA (Coleoptera: Staphylinidae: Aleocharinae). Zootaxa 5165 (4): 575-590, DOI: https://doi.org/10.11646/zootaxa.5165.4.

Myrmedonota xipe Mathis & Eldredge, sp. n.

Myrmedonota xipe Mathis & Eldredge, sp. n. Type series. Holotype, male: MEXICO: Chiapas: Finca Irlanda Biological Station (15 ° 11 ′ N, 92 ° 20 ′ W) 25.ix. 2012, on sticky trap, coll. K. Mathis. Paratypes: 10, same data as holotype. Etymology. The name refers to Xipe Totec, the Aztec life-death-rebirth deity that was worshipped in part by flaying human sacrifices in an act symbolizing the casting off of the old and new growth. The name is a metaphor for the species role in Azteca sericeasur ant societies. The beetles prey on phorid parasitized workers whose deaths reduce phorid fly populations and benefit the colony as a whole (Mathis, in preparation). Diagnosis. This species can be distinguished from all other species of New World Myrmedonota by color pattern, bifid apex of the median lobe, form of the median lobe and copulatory piece. Description. Body (Fig. 5) slender and subparallel. Length with a mean of 3.2 mm (n = 5), color yellowish to black, integument overall dull. Head and abdominal tergites VI–VII dark brown to black; pronotum, elytra, and abdominal tergite V yellow to dark brown; abdominal tergites I–IV yellowish to light brown; mouthparts and legs yellowish; antennae dark brown, segments I–III and apex of segment XI may be yellowish. Legs long; hind tibia 0.78 times as long as the elytral width. Macrosetae prominent; antennal macrosetae 2.47 times the width of the antenomere. Male. Median lobe (Figs. 6–7) somewhat limuloid in parameral view, apex slightly bifid; apical lobe gently curved paramerally in lateral view, generally pointed at apex in lateral and parameral views; longitudinal bands large and conspicuous; copulatory piece overall narrow, apex slender and attenuated, base with lateral paired blunt arms slightly constricted at midpoint, annulus small and longitudinally elongate; comb of teeth present, directed paramerally in lateral view and apical of copulatory piece. Tergite VIII apicomedially concave and margin variably serrate. Female. Spermatheca (Fig. 8) bent submedially at near-right angle. Internal cone with circumventral sculptural grooves.Published as part of Mathis, Kaitlyn A. & Eldredge, K. Taro, 2014, Descriptions of two new species of Myrmedonota Cameron (Staphylinidae: Aleocharinae) from Mexico with comments on the genus taxonomy and behavior, pp. 95-100 in Zootaxa 3768 (1) on pages 98-99, DOI: 10.11646/zootaxa.3768.1.7, http://zenodo.org/record/22611

Myrmedonota Cameron 1920

Genus Myrmedonota Cameron, 1920 Diagnosis. The following character states in combination can diagnose Myrmedonota from other New World genera of Aleocharinae: (1) tarsal formula 4-5 - 5; (2) mesocoxae widely separated; (3) metaventral process much longer than mesoventral process, which extends little between the mesocoxae; (4) galea length greater than 7 times width at base, maxillae overall appearing extremely slender and elongate; (5) neck absent; (6) occipital suture complete to hypostoma; (7) pronotum with complete marginal line; (8) paramerite vellum much larger than condylite vellum; (9) paramerite vellum obscuring condylite vellum from outer view, condylite vellum small and fan-shaped; (9) apical lobe of paramere free and articulating with paramerite; (10) glossa bifid; (11) labial palpomere II and III subequal in length. Comments on taxonomy. Myrmedonota taxonomy is quite chaotic. Elven et al. (2010) demonstrated that Myrmedonota and other New World genera formerly classified under Lomechusini are in fact a lineage within Athetini that has converged on similar morphologies (Elven et al. 2010). Both Lomechusini and these pseudolomechusines are often symbiotic with ants and termites, one potential explanation for convergence may be adaptively rooted in symbiont ecology. Since Elven et al. (2010), more formalized morphological characters that diagnose Lomechusini from pseudolomechusines are becoming apparent (Eldredge personal observation). It is turning out that most New World taxa fall under the currently outdated diagnostic umbrella of Lomechusini are pseudo-lomechusines, and belong to Athetini. This is in contrast to Lomechusini, which are predominantly distributed in the Old World. Therefore, superficially there appears to be a New World-Old World divide in distribution between pseudo-lomechusines and Lomechusini respectively. This is interesting in that it implies there have been two independent evolutionary histories with the lomechusine-morphotype; both have diversified in the context of social insect symbiosis and demonstrate potential for a comparative study of symbiosis. Even with this enlightened perspective of a pseudo-lomechusine lineage, Myrmedonota as currently understood is plesiomorphic in overall body morphology, and many genera may in fact be lineages that have derived from Myrmedonota, rendering it paraphyletic. For example, the genus Termitognathus Borgmier, 1959 may be one such lineage, only diagnosable by morphologies derived from the pressures of living with termites. To attest to the difficulties with distinguishing Myrmedonota from some other pseudo-lomechusine genera, Pace (1997, 2008a, 2008 b, 2009) in a series of publications may have in fact described species of Myrmedonota under Apalonia Casey, 1906 (Eldredge 2012). Habitus and genitalic figures that accompany Pace’s descriptions support this hypothesis. In order to address issues concerning Myrmedonota taxonomy, the new species described below have been compared with Pace’s (1997, 2008a, 2008 b, 2009) descriptions. We bring up these issues on Myrmedonota taxonomy, even though much of the above is still speculative, because we think that Myrmedonota may be phylogenetically important. More apomorphic symbiont lineages may nest within Myrmedonota as we currently diagnose it, making the genus important in understanding the evolution of social insect symbiosis among pseudo-lomechusines. Additionally, this has implications if evolution of social insect symbiosis is to be studied comparatively between Lomechusini and pseudo-lomechusines. We suggest that new genera of pseudo-lomechusines be erected with caution, and urge the phylogeny reconstruction of this diverse clade. Comments on behavior. Observations of Myrmedonota behavior have been accumulating for some time, although most are unpublished. From these, two interesting tendencies have come to light: (1) Myrmedonota swarm to ant colonies, especially during periods of colony agitation; (2) Myrmedonota mate by swarming, frequently in the presence of ants. Myrmedonota are predators, and as ant symbionts either predators of ants (Eldredge personal observation, Mathis in preparation) or scavengers (Kistner 2003). In Costa Rica, Eldredge has observed a Myrmedonota species fly into the midst of an agitated Pheidole Westwood, 1839 colony during nest excavation. Mathis (in preparation) has made detailed observations of aggregation and predation behavior of the two new species described below, but these will be presented subsequently. Mating swarms of M. lewisi Maruyama et al. 2008 have been observed to occur on open ground with no apparent landmark (Eldredge personal observation, http://youtu.be/S 3 cdOavPZmc). Adults would fly above ground and periodically land, at which time they begin a searching behavior until the opposite sex is found. Upon locating a mate, a circular, almost ritualistic chase begins, followed by brief copulation. A white sheet placed on the ground did not elicit concentrated swarming around the sheet, but did allow easier observation of matings. Eldredge also observed mating swarms of a Myrmedonota species in Costa Rica, concentrated around the foraging column of an Eciton Latreille, 1804 species. The two new species described below have been observed mating in the presence of agitated Azteca sericeasur often while Pseudacteon phorid fly attacks took place (Mathis personal observation, http://youtu.be/ 1 IwRT 8 EAp0Y). Adults appear to be attracted to a chemical compound present within the alarm pheromone of Azteca sericeasur (Mathis, in preparation). When the adults arrive to the location and find a mate, a chase begins, often resulting in a lengthy copulation.Published as part of Mathis, Kaitlyn A. & Eldredge, K. Taro, 2014, Descriptions of two new species of Myrmedonota Cameron (Staphylinidae: Aleocharinae) from Mexico with comments on the genus taxonomy and behavior, pp. 95-100 in Zootaxa 3768 (1) on pages 96-97, DOI: 10.11646/zootaxa.3768.1.7, http://zenodo.org/record/22611

Descriptions of two new species of Myrmedonota Cameron (Staphylinidae: Aleocharinae) from Mexico with comments on the genus taxonomy and behavior

Mathis, Kaitlyn A., Eldredge, K. Taro (2014): Descriptions of two new species of Myrmedonota Cameron (Staphylinidae: Aleocharinae) from Mexico with comments on the genus taxonomy and behavior. Zootaxa 3768 (1): 95-100, DOI: 10.11646/zootaxa.3768.1.

Synopsis of the Japanese species of Aleocharinae (Coleoptera: Staphylinidae), with review of the type specimens I. Tribes Himalusini and Leucocraspedini

Maruyama, Munetoshi, Yamamoto, Shûhei, Eldredge, Taro K. (2014): Synopsis of the Japanese species of Aleocharinae (Coleoptera: Staphylinidae), with review of the type specimens I. Tribes Himalusini and Leucocraspedini. Zootaxa 3887 (3): 393-400, DOI: 10.11646/zootaxa.3887.3.