Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly

Abstract

The seasonal cycle varies geographically and organisms are under selection to express life cycles that optimally exploit their spatiotemporal habitats. In insects, this often means producing an annual number of generations (voltinism) appropriate to the local season length. Variation in voltinism may arise from variation in environmental factors (e.g., temperature or photoperiod) acting on a single reaction norm shared across populations, but it may also result from local adaptation of reaction norms. However, such local adaptation is poorly explored at short geographic distances, especially within latitudes. Using a combination of common‐garden rearing and life cycle modeling, we have investigated the causal factors behind voltinism variation in Swedish populations of the butterfly Pararge aegeria, focusing on a set of populations that lie within a single degree of latitude but nonetheless differ in season length and voltinism. Despite considerable differences in ambient temperature between populations, modeling suggested that the key determinant of local voltinism was in fact interpopulation differences in photoperiodic response. These include differences in the induction thresholds for winter diapause, as well as differences in photoperiodic regulation of larval development, a widespread but poorly studied phenomenon. Our results demonstrate previously neglected ways that photoperiodism may mediate insect phenological responses to temperature, and emphasize the importance of local adaptation in shaping phenological patterns in general, as well as for predicting the responses of populations to changes in climate.

Analyzing the neutral and adaptive background of butterfly voltinism reveals structural variation in a core circadian gene

“…Although SNP genotyping of three additional populations revealed a gradient of allele frequencies at the identified candidate loci across the voltinism cline, much variation remained unexplained. Notably, the Gotland island population is bivoltine and exhibits a relatively low critical daylength (Aalberg Haugen & Gotthard, 2015;Lindestad et al, 2019), despite closely resembling the univoltine populations in terms of variation at the 15 candidate loci (Pruisscher et al, 2018). Here we build on these earlier results in several ways.…”

“…The northernmost P. aegeria populations are univoltine; southern populations have many overlapping generations per year and appear not to diapause at all (Nylin et al, 1995). Common-garden studies indicate that this life cycle variation is to a large extent generated by local adaptation of photoperiodic plasticity (Nylin et al, 1995;Lindestad et al, 2019). In mainland Scandinavia, P. aegeria populations shift from univoltine in central Sweden to bivoltine in southern Sweden and Denmark (Fig.…”

“…In contrast, a sufficiently long warm season may permit one or several additional, non-diapausing generations to occur each year (bivoltinism or multivoltinism, respectively). Producing a single versus multiple generations per year is a nontrivial difference, as it may be associated with drastic differences in generation time (Roff, 1980), and may necessitate or drive associated adaptations in terms of regulation of diapause induction (Bean et al, 2012;Lindestad et al, 2019), life history traits such as development rate and body size (Masaki, 1972;Fischer & Fiedler, 2002), and developmental pathway expression (Kivelä et al, 2013;Aalberg Haugen & Gotthard, 2015). Nonetheless, many insect species differ geographically in voltinism, typically in relation to the local length of the warm season (Hart et al, 1997;Braune et al, 2008;Hu et al, 2012;Faccoli & Bernardinelli, 2014;Levy et al, 2015).…”

Developmental trap or demographic bonanza? Opposing consequences of earlier phenology in a changing climate for a multivoltine butterfly

“…Photothermal voltinism (or phenology) models incorporate species-specific thermal windows and photoperiod to evaluate the phenology of multivoltine species (Grevstad & Coop, 2015;Lindestad, Wheat, Nylin, & Gotthard, 2019;Ryan et al, 2018;Tobin, Nagarkatti, Loeb, & Saunders, 2008). These models predict the number of generations a species can fit within a suitable thermal window for a particular region by modeling life history events in response to daylength, temperature, or a combination of both.…”

Developmental plasticity in metabolism but not in energy reserve accumulation in a seasonally polyphenic butterfly

“…Hence, we would expect divergence in life history and physiology to start accumulating immediately after the induction of the developmental pathway, but the developmental timing of trait divergence between diapause and direct development remains insufficiently understood. Depending on species, life history traits start diverging between the alternative developmental pathways either early (Nylin et al, 1989; see also Lindestad et al, 2019) or late in juvenile development (Friberg et al, 2012; Esperk et al, 2013). Development and growth rates are expected to be associated with other biological rates, like metabolic rate (see e.g.…”