Molecular systematics reveals the origins of subsociality in tortoise beetles (Coleoptera, Chrysomelidae, Cassidinae)

Abstract

Subsocial behaviour is known to occur in at least 19 insect orders and 17 families of Coleoptera. Within the leaf beetle family, Chrysomelidae, extended maternal care is reported in only 2 of 15 subfamilies: Cassidinae and Chrysomelinae. Although the emergence of subsociality in insects has received much attention, extensive analyses on the evolution of this behaviour based on phylogenetic approaches are missing. Subsociality is recorded in 33 species of tortoise beetles belonging to the tribes Mesomphaliini and Eugenysini. A molecular phylogenetic reconstruction of these tribes and the remaining five Neotropical tribes of cassidine tortoise beetles was used to investigate the evolution of maternal care and to elucidate the phylogenetic relationships among Neotropical cassidine tribes. A phylogeny was constructed using 90 species and three loci from both mitochondrial and nuclear genes (COI, CAD and 28S). Bayesian inference and maximum likelihood analyses based on a concatenated dataset recovered two independent origins, with no evidence of reversal to solitary behaviour. One origin comprises three Mesomphaliini genera tightly associated with Convolvulaceae, and the other consists of the genus Eugenysa Chevrolat (Eugenysini), a small clade embedded within a group feeding exclusively on Asteraceae. A previous hypothesis suggesting dual origins on different host plants was confirmed, whereas other hypotheses based on a phylogenetic reconstruction of Cassidinae could not be sustained. Our analysis also revealed that the tribe Mesomphaliini is a monophyletic taxon if Eugenysini is included, and for this reason, we re‐establish synonymy of both tribes. We also provide nine new records of subsociality for tortoise beetles species.

Maternal care in Omaspides bistriata Boheman (Coleoptera: Chrysomelidae: Cassidinae: Mesomphaliini)

“…The meticulous care process performed by the mother during the development of the young shows the protection against frequent parasitoids and predators during the egg stage and larval stages, characteristic in several species of Chrysomelidae (Windsor 1987;Choe 1988;Windsor et al 1992;Rodriguez 1994;Kudo & Ishibashi 1995;Chaboo 2002;Gomes et al 2012;Dury et al 2014;Cuozzo et al 2017;Leocádio et al 2020). Intensive care is also evidenced during the pupal stage in which the individuals are totally defenseless, which involves handling and cleaning them (Costa 2006).…”

“…Subsocial behavior encompasses care for offspring by protection against natural enemies, guiding towards or provisioning of food resources during most or all immature stages (Clutton-Brock 1991;Royle et al 2012). Within Coleoptera, subsociality is a rare phenomenon and the behavior has been recorded in 12-17 out of 176 beetle families (Chaboo et al 2014;Leocádio et al 2020). Chrysomelidae Latreille, 1802 is one of the beetle families in which this behavior has evolved indepentently in two subfamilies of 15: Cassidinae Gyllenhal, 1813 and Chrysomelinae Gyllenhal, 1802 (Windsor & Choe 1994;Chaboo et al 2014;Leocádio et al 2020).…”

“…Cassidinae sensu lato is the second largest subfamily of leaf beetles with 6,300 species, distributed worldwide (Borowiec & Świętojańska 2018). Within Cassidinae, parental care has evolved independently in two closely related lineages that feed on distinct host plants families: Asteraceae and Convolvulaceae (Leocádio et al 2020). Until now, parental has been recorded in 24 species belonging to five genera (Chaboo et al 2014;Flinte et al 2015;Macedo et al 2015).…”

New Tachinidae parasitoid records for Mesomphaliini (Coleoptera: Chrysomelidae: Cassidinae) in the Neotropical region

“…Most Mesomphaliini exhibit solitary behavior, but larval gregariousness occurs in subsocial and non-subsocial species (Chaboo et al 2014). Subsocial behavior, displayed as maternal care of immatures, is documented for at least 32 species of three genera of this tribe (not including Eugenysini): Acromis Chevrolat, 1836, Omaspides Chevrolat, 1836, and Paraselenis Spaeth, 1913(Chaboo et al 2014Macedo et al 2015;López-Pérez 2017;Leocádio et al 2020).…”

“…was collected associated with Ipomoea sp. Subsocial behavior is documented for ten species of Paraselenis, including P. flava, an important pest of Ipomoea batatas (sweet potato) in Brazil (Montes and Raga 2010;Chaboo et al 2014;Leocádio et al 2020). Cuignet et al (2008) recorded a species of Eucelatoria (Diptera: Tachinidae) parasitizing Paraselenis tersa (Boheman, 1854) in Panama.…”