Convergent evolution of specialized generalists: Implications for phylogenetic and functional diversity of carabid feeding groups

Abstract

Closely related species are often assumed to be functionally similar. Phylogenetic information is thus widely used to infer functional diversity and assembly of communities. In contrast, evolutionary processes generating functional similarity of phylogenetically distinct taxa are rarely addressed in this context. To investigate the impact of convergent evolution on functional diversity (FD) and phylogenetic diversity (PD), we reconstructed the phylogenetic structure of carabid trophic groups. We then analyzed the mandible shapes using geometric morphometrics to link specialization in functional morphology with feeding specialization among herbivores, generalist carnivores, and specialized consumers of Collembola. Our results show that carabid feeding groups are paraphyletic. Herbivory evolved at least twice and specialization to Collembola predation at least three times. Species within feeding groups share a remarkably similar mandible morphology, which evolved convergently. While specialized mandibles of herbivores and collembolan specialists represent an adaptation to their main food source, the particular mandible morphologies do not necessarily reflect the degree of food specialization within feeding groups. Only a few species with a specialized herbivorous mandible may occasionally feed on animals, but the range of specific food resources in generalist carnivore species is large, despite an almost identical mandible shape. Thus, convergent evolution in specialized feeding groups reverses the relationship between PD and functional similarity compared with generalist carnivores. We conclude that phylogenetic relationship is a poor proxy of FD in carabids. Moreover, the inconsistencies between relatedness, morphological adaptation, and ecological function require caution in the characterization of functional groups. Rather than assuming general relationships between PD and FD, we suggest integrating the analysis of evolutionary processes into functional community analyses.

Evidence for niche conservatism in alpine beetles under a climate‐driven species pump model

“…This pattern likely arises due to the gradual divergence in endophallus features across populations that does not scale with genetic isolation. Ecomorphological functional traits perform well in distinguishing taxa in the N. vandykei species complex, but the weaker performance in distinguishing populations suggests that ecomorphological variation arises over long-term evolutionary divergence, rather than as a result of differential ecological selection in local environments (Baulechner et al, 2020). Very little variation among populations is found in ecophysiological traits, which is in line with previous work showing that physiological traits are highly conserved in Nebria (Slatyer & Schoville, 2016), even among distantly related species.…”

Carabid adaptation to a collembolan diet: hunting efficiency and nutritional value

“…N. biguttatus even outperformed Asaphidion , which has a comparable visual overlap (Bauer, 1985b), in terms of hunting efficiency. Consequently, mandible morphology appears to be the prevailing common trait evolved in carabid collembolan specialists (Baulechner et al ., 2020) and can be used to identify true feeding specialisations in carabids. This is consistent with the observation of a strong link between morphology and dietary specialisation in the animal kingdom (Grant & Grant, 1996; Aguirre et al ., 2002), although mismatches are also common (Bouton et al ., 1998; Ungar et al ., 2008; Brandl et al ., 2015; de Vries et al ., 2016).…”

“…Species of the genus Notiophilus , in contrast, do not possess comparable morphological adaptations, but hunt during the day aided by their highly enlarged eyes. However, common to all species of the genera Loricera , Leistus , and Notiophilus is a convergently evolved specialised mandible shape as an adaptation to hunting collembolans (Baulechner et al ., 2020). Compared to generalist carabids, Collembola specialists show a smaller primary mandibular joint, a more delicate and pointed incisor tooth and lack retinacular ridges (Baulechner et al ., 2020).…”

“…However, common to all species of the genera Loricera , Leistus , and Notiophilus is a convergently evolved specialised mandible shape as an adaptation to hunting collembolans (Baulechner et al ., 2020). Compared to generalist carabids, Collembola specialists show a smaller primary mandibular joint, a more delicate and pointed incisor tooth and lack retinacular ridges (Baulechner et al ., 2020). While these adaptations are most likely responsible for an increased hunting efficiency towards elusive and delicate prey, they hinder consumption of food items requiring high mandible pressure (such as ‘hard’ arthropods or seeds).…”

Integrative taxonomy delimits and diagnoses cryptic arboreal species of the Cyrtodactylus brevipalmatus group (Squamata, Gekkonidae) with descriptions of four new species from Thailand

“…Convergent morphology results from the specific resource requirements that necessitate a particular functional morphology ( Ricklefs 2012 ; Dehling et al 2016 ; Baulechner et al 2020 ). In such cases, phylogenetic analysis becomes paramount to disentangle convergence from common ancestry in order to construct proper phylogenetic taxonomies.…”