Adaptive and maladaptive consequences of “matching habitat choice:” lessons from a rapidly-evolving butterfly metapopulation

Abstract

Relationships between biased dispersal and local adaptation are currently debated. Here, I show how prior work on wild butterflies casts a novel light on this topic. ''Preference'' is defined as the set of likelihoods of accepting particular resources after encountering them. So defined, butterfly oviposition preferences are heritable habitat adaptations distinct from both habitat preference and biased dispersal, but influencing both processes. When a butterfly emigrates after its oviposition preference begins to reduce realized fecundity, the resulting biased dispersal is analogous to that occurring when a fish emigrates after its morphological habitat adaptations reduce its feeding rate. I illustrate preference-biased dispersal with examples from metapopulations of Melitaea cinxia and Euphydryas editha. E. editha were feeding on a well-defended host, Pedicularis, when humans created patches in which Pedicularis was killed and a less-defended host, Collinsia, was rendered phenologically available. Patch-specific natural selection favoured oviposition on Collinsia in logged (''clearing'') patches and on Pedicularis in undisturbed open forest. Quantitative variation in post-alighting oviposition preference was heritable, and evolved to be consistently different between patch types. This difference was driven more by biased dispersal than by spatial variation of natural selection. Insects developing on Collinsia in clearings retained adaptations to Pedicularis in clutch size, geotaxis and oviposition preference, forcing them to choose between emigrating in search of forest habitats with Pedicularis or staying and failing to find their preferred host. Insects that stayed suffered reduction of realized fecundity after delayed oviposition on Collinsia. Those that emigrated suffered even greater fitness penalty from consistently low offspring survival on Pedicularis. Paradoxically, most emigrants reduced both their own fitness and that of the recipient populations by dispersing from a benign natal habitat to which they Electronic supplementary material The online version of this article (

Phenotype‐dependent selection underlies patterns of sorting across habitats: the case of stream‐fishes

“…As mentioned, the mechanisms of non‐random dispersal and phenotype‐dependent habitat choice have only recently started to gain attention and recognition for the role that they play in underlying patterns of species distribution across heterogeneous landscapes. Indeed, while dispersal has long been conceptualized as homogenizing populations (Bolnick et al , Edelaar and Bolnick , Bolnick and Otto , Jacob et al ), recent studies suggest that dispersal is instead non‐random, and along with matching habitat choice may act to strengthen and help produce local adaptations and among‐habitat differentiation (Edelaar et al , Bolnick et al , Edelaar and Bolnick , Bolnick and Otto , Richardson et al , Singer ), at even small spatial scales (Bolnick et al , Richardson et al ). While other habitat preference mechanisms exist and can also lead to patterns of phenotype– habitat sorting, natal imprinting for example forming correlations across generations through local selection, our findings support the action of matching habitat choice for several key reasons.…”

“…Here we use the definition of matching habitat choice as per Singer (), which relaxes the requirement that individuals act to increase their expected fitness (although see model analysis), as we did not empirically measure if individual fitness increased as the result of habitat choice decisions. While this may be inferred based on functional interpretations of the trait– habitat relationships resulting from such decisions, future work should also investigate if individual habitat choice decisions are repeatable and if indeed fitness is increased following such decisions (elements 3 and 4 in Edelaar et al ).…”

“…Alternatively, however, correlations may arise when phenotypes remain constant but individuals alter the environmental conditions in which they are located (i.e. move or disperse, small or large scale, respectively) (Edelaar et al , Bolnick and Otto , Camacho et al , Jacob et al , Singer ). Two mechanisms, non‐random dispersal (movement) and matching habitat choice/phenotype‐dependent habitat selection (see Edelaar et al for a list of alternate terms), underlie this process.…”

Phenological matching rather than genetic variation in host preference underlies geographical variation in host plants used by orange tip butterflies

“…In addition to the factors relating to the plant, a female's own state may influence her host plant choice. For example, egg load, search time, and experienced abundance and quality of different host plant species can influence the oviposition choice (Minkenberg, Tatar & Rosenheim, 1992;West & Cunningham, 2002;Singer, 2015).…”

Attraction of Melitaea cinxia Butterflies to Previously-Attacked Hosts: A Likely Complement to Known Allee Effects?

“…In contrast, they were clearly and genetically different in oviposition preference (Kuussaari et al 2000). The adaptive significance of this differentiation is not known, but if it exists it is probably connected with hostfinding efficiency (Singer 2015).…”