The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae).

In order to facilitate the study of the evolution of female flightlessness among the geometrid subfamily Ennominae (Lepidoptera, Geometridae), we carried out a phylogenetic analysis based on a morphological data matrix, and DNA sequences. We used seven nuclear gene fragments, elongation factor 1alpha (EF-1alpha), wingless (wgl), isocitrate dehydrogenase (IDH), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), ribosomal protein S5 (RpS5) and segments D1 and D2 of the 28S rRNA gene, and one mitochondrial gene fragment, cytochrome oxidase subunit I (COI). Sampling included 55 species of Ennominae covering all tribes with flightless females of the Holarctic boreal zone, and some other geometrids used as outgroups. Our results clearly confirmed that Ennominae (including Alsophila of the traditional subfamily Alsophilinae) is a monophyletic group, as well as supported the previously established morphology-based division of Ennominae into "ennomine" and "boarmiine" groups of genera. A number of taxonomic ambiguities were resolved but the monophyly of the traditionally recognised tribe Bistonini, comprising a number of flightless species, remained ambiguous. Bistonini is thus suggested to be subsumed to the tribe Boarmiini in the broad sense. Indeed, an analysis of timing of divergence suggested that Boarmiini s. lat. rapidly diversified in the late Oligocene/early Miocene. Within the Ennominae, seven independent origins of female flightlessness were revealed facilitating phylogenetic comparative analyses to be performed in search of causes and consequences of this phenomenon. The present phylogenetic hypothesis supports the conclusions of the "adaptive story", a hypothesis of the sequence of evolutionary events leading to flightlessness, we have presented earlier (Snäll et al., 2007). In particular, in the "boarmiine" group, the tribe Boarmiini s. lat. clearly represents a group of geometrids in which female flightlessness has evolved more frequently than in any other tribes, suggesting that this clade has likely been predisposed to evolutionary events leading to the manifestation of female flightlessness. The ancestor of the wing-reduced Ennominae has likely been a winged but slow flying forest moth feeding polyphagously on deciduous trees.