The genomic and cellular basis of biosynthetic innovation in rove beetles.

How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland-a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization-most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.

The genomic and cellular basis of biosynthetic innovation in rove beetles.

How evolution at the cellular level potentiates change at the macroevolutionary level is a major question in evolutionary biology. With >66,000 described species, rove beetles (Staphylinidae) comprise the largest metazoan family. Their exceptional radiation has been coupled to pervasive biosynthetic innovation whereby numerous lineages bear defensive glands with diverse chemistries. Here, we combine comparative genomic and single-cell transcriptomic data from across the largest rove beetle clade, Aleocharinae. We retrace the functional evolution of two novel secretory cell types that together comprise the tergal gland-a putative catalyst behind Aleocharinae's megadiversity. We identify key genomic contingencies that were critical to the assembly of each cell type and their organ-level partnership in manufacturing the beetle's defensive secretion. This process hinged on evolving a mechanism for regulated production of noxious benzoquinones that appears convergent with plant toxin release systems, and synthesis of an effective benzoquinone solvent that weaponized the total secretion. We show that this cooperative biosynthetic system arose at the Jurassic-Cretaceous boundary, and that following its establishment, both cell types underwent ∼150 million years of stasis, their chemistry and core molecular architecture maintained almost clade-wide as Aleocharinae radiated globally into tens of thousands of lineages. Despite this deep conservation, we show that the two cell types have acted as substrates for the emergence of adaptive, biochemical novelties-most dramatically in symbiotic lineages that have infiltrated social insect colonies and produce host behavior-manipulating secretions. Our findings uncover genomic and cell type evolutionary processes underlying the origin, functional conservation and evolvability of a chemical innovation in beetles.

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

A new genus and species, Myrmecoagria hoebekei is described as the first known myrmecophilous representative of Falagriini in North America. The new species is believed to be associated with Myrmica ants based on an associated host specimen and label data. Ahn Ashes (1995) dataset is modified to investigate the placement of Myrmecoagria and evolution of myrmecophily within Falagriini. Sceptobiini, a long suspected close relative of Falagriini was included in the analysis and was recovered nested within Falagriini. Myrmecoagria was recovered distant to Myrmecopora, a genus with anatomical similarities.

Response to "Evidence from amber for the origins of termitophily".

In a recent Current Biology paper [1], we reported the oldest, morphologically specialized, and obligate termitophiles, Cretotrichopsenius burmiticus (Figure 1, left), from mid-Cretaceous Burmese amber, about 99 million years old. Cretotrichopsenius, belonging to the obligately termitophilous rove beetle tribe Trichopseniini, display the protective horseshoe-crab-shaped body typical of many extant termitophiles. However, the termitophilous lifestyle of Cretotrichopsenius is being questioned by Yamamoto et al.[2] based on their representation of the termitophile-related features and premature and presumptive phylogenetic placement of Cretotrichopsenius within Trichopseniini. We stand by our interpretation that Cretotrichopsenius are obligate termitophiles, and Mesosymbion[3], a member of the largely free-living Mesoporini, are not necessarily termitophilous.

Early Evolution of Specialized Termitophily in Cretaceous Rove Beetles.

Termitophiles, symbionts that live in termite nests, include a wide range of morphologically and behaviorally specialized organisms. Complex adaptive mechanisms permit these animals to integrate into societies and to exploit their controlled physical conditions and plentiful resources, as well as to garner protection inside termite nests. An understanding of the early evolution of termitophily is challenging owing to a scarcity of fossil termitophiles, with all known reliable records occurring from the Miocene (approximately 19 million years ago [mya]) [1-6], and an equivocal termitophile belonging to the largely free-living Mesoporini from the mid-Cretaceous [7]. Here we report the oldest, morphologically specialized, and obligate termitophiles from mid-Cretaceous Burmese amber (99 mya). Cretotrichopsenius burmiticus gen. et sp. nov. belongs to Trichopseniini, a group of distinctive termitophilous aleocharine rove beetles, all of which possess specialized swollen or horseshoe-crab-shaped body plans. Cretotrichopsenius display the protective horseshoe-crab-shaped body form typical of many modern termitophiles, with concealed head and antennae and strong posteriorly directed abdominal setae. Cretotrichopsenius represent the earliest definitive termitophiles, shedding light on host associations in the early evolution of termite societies. The fossil reveals that ancient termite societies were quickly invaded by beetles and by multiple independent lineages of social parasites over the subsequent eons.

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

Two new species of Myrmedonota, M. shimmerale n. sp. and M. xipe n. sp., are described, and the genus is recorded from Mexico for the first time. Dorsal habitus photographs, illustrations of the median lobe and spermatheca are presented for diagnostic purposes. We suggest that Myrmedonota is in fact diverse in the New World and that its taxonomy is already in a state of confusion. New behavioral observations show that: (1) Myrmedonota species will aggregate towards agitated ants, possibly to prey on them; (2) Myrmedonota will form mating swarms, either with no apparent landmark or in the vicinity of ants.

Two new genera and species of the termite symbiont lineage Termitohospitini (Coleoptera, Staphylinidae, Aleocharinae) from Bolivia and peninsular Malaysia.

Coptotermocola clavicornisgen. & sp. n. and Neotermitosocius bolivianusgen. & sp. n. of the termite inquilinous tribe Termitohospitini are described from peninsular Malaysia and Bolivia, respectively. The Termitohospitini are most readily diagnosable by the distally migrated anterior tentorial pits that are no longer associated with the antennal fossae, and by the enlarged vertex which obscures the antennal fossae dorsally. Additionally, the Termitohospitini are hypothesized to share a recent common ancestor with the Masuriini and Myllaenini due to shared derived morphologies of the lacinia distal teeth with lateral cuticular processes, presence of a unique maxillary palpomere III sensilla, and anterolateral angles of mentum produced. Habitus photographs and illustrations of diagnostic features are provided for the two new genera in order to facilitate future work.