Phylogenomics supports localized and taxonomically-incongruous ecological specialization in a North American moth clade (the Hemileuca maia species complex)

Authors: DUPUIS, JULIAN - University Of Hawaii; PEIGLER, RICHARD - University Of Incarnate Word; Geib, Scott; RUBINOFF, DANIEL - University Of Hawaii

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2018
Publication Date: 9/29/2018
Citation: Dupuis, J.R., Peigler, R.S., Geib, S.M., Rubinoff, D. 2018. Phylogenomics supports localized and taxonomically-incongruous ecological specialization in a North American moth clade (the Hemileuca maia species complex). Molecular Ecology. 27:4417-4429. https://doi.org/10.1111/mec.14883.
DOI: https://doi.org/10.1111/mec.14883

Interpretive Summary: Populations adapting to specific local conditions (having higher fitness in their natal habitats than in the habitats of other populations) can often be one of the first stages in the process of ecological speciation. However, when populations are still connected with gene flow, the dynamics of local adaptation and its outcome (i.e. speciation or not) are not necessarily straightforward. Here, we investigate local adaptation and population genomic structure in a species group of charismatic, day-flying moths. These moths show high variation in morphology and ecology, but many populations are clearly adapted to specific host plants and habitats, and previous studies have found that there is very little genetic differentiation across all of North America. We generate the first genomic dataset for this group, and for the first time, find genetic differentiation between populations. Some of this genetic structure seems to be related to host plant and habitat specialization, but not all of it. These results call into question the current taxonomy of the group, which is important because several species and recognized forms are protected at the state/provincial and federal level in the USA and Canada. This system provides a model to study local adaptation, and gives great insight into how ecological specialization can foster the creation of biodiversity in the face of gene flow.

Technical Abstract: Local adaptation can be a fundamental component of speciation, but its dynamics in relation to gene flow are not necessarily straightforward. Herbivorous taxa with localized host plant or habitat specialization across their geographic range are ideal models for investigating the patterns and constraints of local adaptation and its impact on diversification. The charismatic, day-flying moths of the Hemileuca maia species complex (Lepidoptera: Saturniidae) are such taxa, as they are geographically-widespread, exhibit considerable ecological and morphological variability and host and habitat specificity, but apparently lack genetic differentiation across their range. Here, we use genome-wide single nucleotide polymorphisms to assess relationships and population genomic structure of this group across North America, and investigate the scales at which genomic divergence correlates with adaptive ecological characteristics. In contrast to all previous genetic studies of the group, we find both broad- and fine-scale genetic differentiation between lineages, which is at odds with various levels of taxonomic description and recognition of conservation units. Furthermore, ecological specialization only explains some of the finest-scale genetic differentiation, and across much of the group’s range, local adaptation is apparently occurring in the face of strong gene flow. This system provides a model for understanding both how local adaptation in an herbivore can arise and be maintained in the face of apparently strong gene flow, and the importance of geographic isolation in generating broader genomic divergence, despite a lack of ecological divergence.