Ultraconserved Elements Reveal the Relationship Between Facultative Keratinophagy and Synanthropic Evolution in Clothes Moths

Synanthropic species live in close association with, or benefit from, humans. Despite their potential impacts to human health, little is known about the mechanisms driving synanthropic life-history evolution, evolutionary forces shaping diet among synanthropes, or how these combined factors affect population dynamics and/or speciation. The Tineidae moth family contains several synanthropic species, including the globally distributed pest species Tineola bissellellia, that contribute to the ~$1 billion worth of damage caused annually by keratinophagous synanthropes. Synanthropy among Tineidae is associated with a wide range of dietary strategies. While most tineids display obligate detritivory, synanthropic species are typically either facultatively or obligately keratinophagous. However, little is known about evolutionary relationships within Tineidae, hampering efforts to investigate the relationship between synanthropy and diet evolution. Here, to address this challenge, we extracted DNA from 39 tineid samples and two outgroups, including the closely related Tineola and Tinea genera, and generated genome-wide sequence data for thousands of ultraconserved elements (UCEs). Our phylogenetic analyses, using a concatenated maximum-likelihood-based approach, resulted in a well-supported, fully resolved phylogeny that demonstrates synanthropy has evolved multiple times and is consistently associated with facultative and obligate keratinophagy. Bayesian divergence time estimation indicates Cretaceous divergence among deep-branching tineid lineages, an ancestral origin of facultative keratinophagy, and a recent origin of the most economically important synanthropic pest, Tineola bissellellia, from within genus Tinea. Taken together, our results suggest that a shift to facultative keratinophagy was a key evolutionary innovation that has fuelled the repeated evolution of synanthropic life histories among this deep-diverging moth family.