Diana Posledovich

Climate change, phenology, and butterfly host plant utilization

Knowledge of how species interactions are influenced by climate warming is paramount to understand current biodiversity changes. We review phenological changes of Swedish butterflies during the latest decades and explore potential climate effects on butterfly–host plant interactions using the Orange tip butterfly Anthocharis cardamines and its host plants as a model system. This butterfly has advanced its appearance dates substantially, and its mean flight date shows a positive correlation with latitude. We show that there is a large latitudinal variation in host use and that butterfly populations select plant individuals based on their flowering phenology. We conclude that A. cardamines is a phenological specialist but a host species generalist. This implies that thermal plasticity for spring development influences host utilization of the butterfly through effects on the phenological matching with its host plants. However, the host utilization strategy of A. cardamines appears to render it resilient to relatively large variation in climate.

Latitudinal variation in diapause duration and post-winter development in two pierid butterflies in relation to phenological specialization

Diapause plays a central role in insect life cycles by allowing survival during adverse seasonal conditions as well as synchronizing life cycles with the period of mate and food availability. Seasonal timing is expected to be particularly important for species that are dependent on resources available during a short time window—so-called phenological specialists—and latitudinal clines in seasonality are expected to favor local adaptation in phenological timing. However, to what degree latitudinal variation in diapause dynamics and post-winter development due to such local adaptation is influenced by the degree of phenological specialization is not well known. We experimentally studied two pierid butterfly species and found that the phenological specialist Anthocharis cardamines had shorter diapause duration than the phenological generalist Pieris napi along a latitudinal gradient in Sweden. Moreover, diapause duration increased with latitude in P. napi but not in A. cardamines. Sensitivity of the two species to winter thermal conditions also differed; additional cold temperature during the winter period shortened diapause duration for P. napi pupae but not for A. cardamines pupae. In both species, post-winter pupal development was faster after longer periods of cold conditions, and more southern populations developed faster than northern populations. Post-winter development was also invariably faster at higher temperatures in both species. We argue that the observed differences in diapause dynamics between the two species might be explained by the difference in phenological specialization that influences the costs of breaking diapause too early in the season.

Decoupling of female host plant preference and offspring performance in relative specialist and generalist butterflies

The preference-performance hypothesis posits that the host plant range of plant-feeding insects is ultimately limited by larval costs associated with feeding on multiple resources, and that female egg-laying preferences evolve in response to these costs. The trade-off of either using few host plant species and being a strong competitor on them due to effective utilization or using a wide host plant range but being a poor competitor is further predicted to result in host plant specialization. This follows under the hypothesis that both females and offspring are ultimately favoured by utilizing only the most suitable host(s). We develop an experimental approach to identify such trade-offs, i.e. larval costs associated with being a host generalist, and apply a suite of experiments to two sympatric and syntopic populations of the closely related butterflies Pieris napi and Pieris rapae. These butterflies show variation in their level of host specialization, which allowed comparisons between more and less specialized species and between families within species. Our results show that, first, the link between female host preference and offspring performance was not significantly stronger in the specialist compared to the generalist species. Second, the offspring of the host plant specialist did not outperform the offspring of the generalist on the former’s most preferred host plant species. Finally, the more generalized species, or families within species, did not show higher survival or consistently higher growth rates than the specialists on the less preferred plants. Thus, the preference and performance traits appear to evolve as largely separated units.

The developmental race between maturing host plants and their butterfly herbivore – the influence of phenological matching and temperature

Interactions between herbivorous insects and their host plants that are limited in time are widespread. Therefore, many insect-plant interactions result in a developmental race, where herbivores need to complete their development before plants become unsuitable, while plants strive to minimize damage from herbivores by outgrowing them. When spring phenologies of interacting species change asymmetrically in response to climate warming, there will be a change in the developmental state of host plants at the time of insect herbivore emergence. In combination with altered temperatures during the subsequent developmental period, this is likely to affect interaction strength as well as fitness of interacting species. Here, we experimentally explore whether the combined effect of phenological matching and thermal conditions influence the outcome of an insect-host interaction. We manipulated both developmental stages of the host plants at the start of the interaction and temperature during the subsequent developmental period in a model system of a herbivorous butterfly, Anthocharis cardamines, and five of its Brassicaceae host plant species. Larval performance characteristics were favoured by earlier stages of host plants at oviposition as well as by higher developmental temperatures on most of the host species. The probability of a larva needing a second host plant covered the full range from no influence of either phenological matching or temperature to strong effects of both factors, and complex interactions between them. The probability of a plant outgrowing a larva was dependent only on the species identity. This study demonstrates that climatic variation can influence the outcome of consumer-resource interactions in multiple ways and that its effects differ among host plant species. Therefore, climate warming is likely to change the temporal match between larval and plant development in some plant species, but not in the others. This is likely to have important implications for host plant use and possibly influence competitive relationships.

Variation in two phases of post-winter development of a butterfly

The temporal aspects of life cycle characteristics, such as diapause development, are under strong selection in seasonal environments. Fine‐tuning of the life cycle may be particularly important to match the phenology of potential mates and resources as well as for optimizing abiotic conditions at eclosion. Here, we experimentally study the spring phenology of the orange tip butterfly, Anthocharis cardamines, by analysing post‐winter pupal development in three populations along a latitudinal cline in each of Sweden and the United Kingdom. These countries differ substantially in their seasonal temperature profile. By repeatedly recording pupal weights, we established that post‐winter development has two separate phases, with a more rapid weight loss in the second phase than in the first, likely corresponding to a ramping up of the rate of development. Variation in the duration of the first phase contributed more strongly than the second phase to the differences in phenology between the localities and sexes. We found that insects from Sweden had a faster overall rate of development than those from the United Kingdom, which is consistent with countergradient variation, as Sweden is colder during the spring than the United Kingdom. Similar trends were not observed at the within‐country scale, however. A cogradient pattern was found within Sweden, with populations from the north developing more slowly, and there was no clear latitudinal trend within the United Kingdom. In all localities, males developed faster than females. Our results point to the importance of variation in the progression of post‐winter development for spring phenology.

Energy and lipid metabolism during direct and diapause development in a pierid butterfly

ABSTRACT Diapause is a fundamental component of the life cycle in the majority of insects living in environments characterized by strong seasonality. The present study addresses poorly understood associations and trade-offs between endogenous diapause duration, thermal sensitivity of development, energetic cost of development and cold tolerance. Diapause intensity, metabolic rate trajectories and lipid profiles of directly developing and diapausing animals were studied using pupae and adults of Pieris napi butterflies from a population in which endogenous diapause has been well studied. Endogenous diapause was terminated after 3 months and termination required chilling. Metabolic and post-diapause development rates increased with diapause duration, while the metabolic cost of post-diapause development decreased, indicating that once diapause is terminated, development proceeds at a low rate even at low temperature. Diapausing pupae had larger lipid stores than the directly developing pupae, and lipids constituted the primary energy source during diapause. However, during diapause, lipid stores did not decrease. Thus, despite lipid catabolism meeting the low energy costs of the diapausing pupae, primary lipid store utilization did not occur until the onset of growth and metamorphosis in spring. In line with this finding, diapausing pupae contained low amounts of mitochondria-derived cardiolipins, which suggests a low capacity for fatty acid β-oxidation. While ontogenic development had a large effect on lipid and fatty acid profiles, only small changes in these were seen during diapause. The data therefore indicate that the diapause lipidomic phenotype is developed early, when pupae are still at high temperature, and retained until post-diapause development. Summary: Diapause termination in Pieris napi requires chilling, energy is stored for post-diapause purposes and the diapause lipidome is distinct but lacks dynamics during diapause development.

Plant-herbivore synchrony and selection on plant flowering phenology.

Temporal variation in natural selection has profound effects on the evolutionary trajectories of populations. One potential source of variation in selection is that differences in thermal reaction norms and temperature influence the relative phenology of interacting species. We manipulated the phenology of the butterfly herbivore Anthocharis cardamines relative to genetically identical populations of its host plant, Cardamine pratensis, and examined the effects on butterfly preferences and selection acting on the host plant. We found that butterflies preferred plants at an intermediate flowering stage, regardless of the timing of butterfly flight relative to flowering onset of the population. Consequently, the probability that plant genotypes differing in timing of flowering should experience a butterfly attack depended strongly on relative phenology. These results suggest that differences in spring temperature influence the direction of herbivore-mediated selection on flowering phenology, and that climatic conditions can influence natural selection also when phenotypic preferences remain constant.