Molecular phylogenetics and evolution of maternal care in Membracine treehoppers.

The treehopper subfamily Membracinae (Insecta: Hemiptera: Membracidae) comprises the majority of genera and species diversity in the New World tropics. These treehoppers exhibit a wide range of social behaviors, making them an excellent group for studying patterns of social evolution in insects. However, to date the tribal and generic relationships have remained unclear. We reconstructed the phylogeny of the Membracinae using a combined mitochondrial (COI, COII, tRNA-Leu, and 12S) and nuclear (Wg) gene data set. A total of 2608 aligned nucleotide sites were obtained for 112 species, representing 25 of 38 currently recognized genera and all four tribes. A strict consensus of five equally parsimonious trees recovered the subfamily and three of its four tribes. The majority rule consensus tree derived from the Bayesian analyses based on the GTR+I+G and mixed-models recovered many clades shared with the parsimony trees and is identical to the single best tree inferred from maximum likelihood analysis, aside from the rearrangement of one node. A comparison of mitochondrial and nuclear genes indicated that Wg provided higher consistency index (CI), data decisiveness (DD), partitioned Bremer support (PBS) than any of the mitochondrial genes analyzed. The combined mitochondrial and nuclear DNA provide strong support for the monophyly of the subfamily and three of its four tribes (Aconophorini, Hoplophorionini, and Hypsoprorini). Membracini is paraphyletic with respect to Hoplophorionini and contains two lineages, the Membracini sensu strictu and the newly resurrected tribe Bolbonotini. Our analyses show that there is a strong phylogenetic component to the evolution of maternal care. Given the widespread occurrence of maternal care within the subfamily, this trait is estimated to have ≤3 origins, two reversals, and one loss. Our results suggest that the evolution of maternal care in insects may not be as evolutionarily labile as previously thought. (Bayesian analysis; maximum likelihood; Membracidae; mitochondrial gene; nuclear gene; phylogeny; social evolution; treehoppers.) Treehoppers in the family Membracidae (Insecta: Hemiptera) exhibit diversity in behavioral and life his- tory traits including maternal care (subsociality), ant mu- tualism, host-plant specialization and plant-borne vi- brational communication (Wood, 1993; Cocroft, 1996, 2001). The New World treehopper subfamily Membraci- nae (Fig. 1) has a mostly Neotropical distribution, with the highest generic and species diversity in the tropical regions of Central America and northern South America on the eastern slope of Andes adjacent to the edge of Amazon basin (Metcalf and Wade, 1965; Wood, 1993; McKamey, 1998). Members of the subfamily exhibit vari- ation in social behavior ranging from solitary individu- als, nymphal or adult aggregations to highly developed maternal care with parent-offspring communication (Wood, 1993; Cocroft, 1996, 1999). The variation in so- cial behavior among closely related species within the Membracinae provides an excellent opportunity for ad- dressing a number of important questions in insect social evolution. Does the evolution of maternal care rep- resent a convergent adaptation to ecological conditions, reflect phylogenetic patterns, or both? How frequently has this behavior evolved, and how easily can it be lost once developed? Treehoppers provide some of the best-studied exam- ples of subsocial behavior in insects. Subsocial behav- ior in treehoppers is restricted to maternal care of eggs and nymphs. Egg-guarding is the most common form of maternal care in treehoppers and is defined as a fe-