Analysis of the Function and Evolution of Mite Pockets in Lizards.

Abstract

Numerous lizard species possess mite pockets – dermal invaginations inhabited by ectoparasitic mites, particularly chiggers (Trombiculidae, Leeuwenhoekiidae). Pockets shelter mites, and chiggers preferentially attach within pockets. However, it remains unclear how lizards benefit from this association. In the present study, associations between mites, pockets, and hosts in the Phrynosomatidae were examined using phylogenetically-independent comparative methods and ancestral state reconstructions, and hypotheses for pocket function experimentally tested using Sceloporus jarrovi (Phrynosomatidae). Mite infestations in S. jarrovi varied greatly between host demographic groups. Chiggers concentrated within the nuchal pocket in all groups, and pocket capacity was limited by host body size. Ectoparasitism significantly impaired growth in juveniles but had no effect on adult body condition. Examination of museum specimens representing 77 phrynosomatid species revealed similar patterns of ectoparasitism. Nuchal pockets occurred in 70 species; post-inguinal pockets in only 14. Chiggers consistently concentrated in the pockets despite variation in host species morphology and ecology. Comparative analysis revealed mite loads to be positively correlated with pocket size and habitat, and negatively with latitude. Pocket morphology varied considerably, displaying significant positive associations with body size and rugosity, and negative with latitude. Damage-amelioration and mate choice hypotheses for pocket function were experimentally tested using S. jarrovi. Damage-amelioration proposes pockets reduce and/or repair mite damage. Histomorphometric analyses indicate pocket tissues differ morphologically from non-pockets but do not reduce or rapidly repair damage. Instead, pockets likely reduce mite feeding efficiency and/or reduce host irritation by limiting mite damage to the superficial tissues. The mate choice hypothesis proposes pockets conceal ectoparasites from conspecifics. In mate choice trials female S. jarrovi appeared to choose males randomly; neither ectoparasite burden nor male morphology had a significant influence on female choice, and the mate choice hypothesis was not supported. Ancestral state reconstructions suggest the ancestor of Phrynosomatidae had small nuchal pockets, no post-inguinal pockets, and modest mite loads. Nuchal pockets were independently lost in Callisaurini and Uta, possibly due to specialization for arid habitats. Expansion and diversification of Sceloporus into moist, low latitude, high elevation habitats with dense mite populations coincided with enlargement of nuchal pockets, suggestive of mite-related function.