The genetic and ecological factors that shape the evolution of animal diets remain poorly understood. For herbivorous insects, the expectation has been that trade-offs exist, such that adaptation to one host plant reduces performance on other potential hosts. We investigated the genetic architecture of alternative host use by rearing individual Lycaeides melissa butterflies from two wild populations in a crossed design on two hosts (one native and one introduced) and analysing the genetic basis of differences in performance using genomic approaches. Survival during the experiment was highest when butterfly larvae were reared on their natal host plant, consistent with local adaptation. However, cross-host correlations in performance among families (within populations) were not different from zero. We found that L. melissa populations possess genetic variation for larval performance and variation in performance had a polygenic basis. We documented very few genetic variants with trade-offs that would inherently constrain diet breadth by preventing the optimization of performance across hosts. Instead, most genetic variants that affected performance on one host had little to no effect on the other host. In total, these results suggest that genetic trade-offs are not the primary cause of dietary specialization in L. melissa butterflies.

Animals often express behavioral preferences for different types of food or other resources, and these preferences can evolve or shift following association with novel food types. Shifts in preference can involve at least two phenomena: a change in rank preference or a change in specificity. The former corresponds to a change in the order in which hosts are preferred, while a shift in specificity can be an increase in the tendency to utilize multiple hosts. These possibilities have been examined in relatively few systems that include extensive population-level replication. The Melissa blue butterfly, Lycaeides melissa, has colonized exotic alfalfa, Medicago sativa, throughout western North America. We assayed the host preferences of 229 females from ten populations associated with novel and native hosts. In four out of five native-associated populations, a native host was preferred over the exotic host, while preference for a native host characterized only two out of five of the alfalfa-associated populations. Across all individuals from alfalfa-associated populations, there appears to have been a decrease in specificity: females from these populations lay fewer eggs on the native host and more eggs on the exotic relative to females from native-host populations. However, females from alfalfa-associated populations did not lay more eggs on a third plant species, which suggests that preferences for specific hosts in this system can potentially be gained and lost independently. Geographic variation in oviposition preference in L. melissa highlights the value of surveying a large number of populations when studying the evolution of a complex behavioral trait.

The role of ecology in diversification has been widely investigated, though few groups have been studied in enough detail to allow comparisons of different ecological traits that potentially contribute to reproductive isolation. We investigated larval performance within a species complex ofLycaeidesbutterflies. Caterpillars from seven populations were reared on five host plants, asking if host-specific, adaptive larval traits exist. We found large differences in performance across plants and fewer differences among populations. The patterns of performance are complex and suggest both conserved traits (i.e., plant effects across populations) and more recent dynamics of local adaptation, in particular forL. melissathat has colonized an exotic host. We did not find a relationship between oviposition preference and larval performance, suggesting that preference did not evolve to match performance. Finally, we put larval performance within the context of several other traits that might contribute to ecologically based reproductive isolation in theLycaeidescomplex. This larger context, involving multiple ecological and behavioral traits, highlights the complexity of ecological diversification and emphasizes the need for detailed studies on the strength of putative barriers to gene flow in order to fully understand the process of ecological speciation.

The colonization of exotic plants by herbivorous insects has provided opportunities for investigating causes and consequences of the evolution of niche breadth. The butterfly Lycaeides melissa utilizes exotic alfalfa, Medicago sativa, which is a relatively poor larval resource, and previous studies have found that caterpillars that consume M. sativa develop into smaller and less fecund adults. Here we investigate the effect of smaller female body size on male mate preference, a previously unexplored consequence of novel host use. Smaller females, which developed on the exotic host, were less likely to be visited by males. This result was confirmed with a second set of choice tests involving females reared on a single plant species, thus ruling out host-specific confounding factors. We suggest that an effect on mate choice be considered part of the complex suite of factors determining persistence of herbivorous insects following colonization of new habitats or resources.

1. Interactions among caterpillars, ants and parasitoids have informed much of what is known about tritrophic ecological dynamics. However, detailed studies encompassing all three trophic levels are limited to relatively few natural systems. In this study, interactions of the Melissa blue butterfly, Lycaeides melissa, with mutualistic ants and parasitoids in the context of novel host plant use by the butterfly were investigated.2. Over the course of 2 years, 526 caterpillars and 288 ants tending caterpillars were collected from 185 plants at sites with two different native host plants and the exotic host alfalfa, for the purpose of investigating if the presence of ants was associated with reduced rates of parasitism.3. The abundance and diversity of parasitoids varied considerably across space and time. The presence of tending ants did not appear to reduce rates of parasitism, in contrast to a previous study of L. melissa, which found evidence of ant protection against spiders and other predators.4. This study has increased our understanding of ant-caterpillar-enemy interactions, and previously unobserved interactions have been documented, including at least two new host-parasitoid relationships. These findings highlight the importance of investigating ecological interactions, including interactions with other trophic levels, when studying diet breadth and ecological diversification in herbivorous insects.