Strategies of chemical anti-predator defences in leaf beetles: is sequestration of plant toxins less costly than de novo synthesis?

The evolution of defensive traits is driven both by benefits gained from protection against enemies and by costs of defence production. We tested the hypothesis that specialisation of herbivores on toxic host plants, accompanied by the ability to acquire plant defensive compounds for herbivore defence, is favoured by the lower costs of sequestration compared to de novo synthesis of defensive compounds. We measured physiological costs of chemical defence as a reduction in larval performance in response to repeated removal of secretions (simulating predator attack) and compared these costs between five species synthesising defences de novo and three species sequestering salicylic glucosides (SGs) from their host plants. Experiments simulating low predator pressure revealed no physiological costs in terms of survival, weight and duration of development in any of study species. However, simulation of high predation caused reduction in relative growth rate in Chrysomela lapponica larvae producing autogenous defences more frequently, than in larvae sequestering SGs. Still meta-analysis of combined data showed no overall difference in costs of autogenous and sequestered defences. However, larvae synthesising their defences de novo demonstrated secretion-conserving behaviour, produced smaller amounts of secretions, replenished them at considerably lower rates and employed other types of defences (regurgitation, evasion) more frequently when compared to sequestering larvae. These latter results provide indirect evidence for biosynthetic constraints for amounts of defensive secretions produced de novo, resulting in low defence effectiveness. Lifting these constraints by sequestration may have driven some leaf beetle lineages toward sequestration of plant allelochemicals as the main defensive strategy.

Climate shapes the spatiotemporal variation in color morph diversity and composition across the distribution range of Chrysomela lapponica leaf beetle.

Color polymorphism offers rich opportunities for studying the eco-evolutionary mechanisms that drive the adaptations of local populations to heterogeneous and changing environments. We explored the color morph diversity and composition in a Chrysomela lapponica leaf beetle across its entire distribution range to test the hypothesis that environmental and climatic variables shape spatiotemporal variation in the phenotypic structure of a polymorphic species. We obtained information on 13 617 specimens of this beetle from museums, private collections, and websites. These specimens (collected from 1830-2020) originated from 959 localities spanning 33° latitude, 178° longitude, and 4200 m altitude. We classified the beetles into five color morphs and searched for environmental factors that could explain the variation in the level of polymorphism (quantified by the Shannon diversity index) and in the relative frequencies of individual color morphs. The highest level of polymorphism was found at high latitudes and altitudes. The color morphs differed in their climatic requirements; composition of colour morphs was independent of the geographic distance that separated populations but changed with collection year, longitude, mean July temperature and between-year temperature fluctuations. The proportion of melanic beetles, in line with the thermal melanism hypothesis, increased with increasing latitude and altitude and decreased with increasing climate seasonality. Melanic morph frequencies also declined during the past century, but only at high latitudes and altitudes where recent climate warming was especially strong. The observed patterns suggest that color polymorphism is especially advantageous for populations inhabiting unpredictable environments, presumably due to the different climatic requirements of coexisting color morphs.

Climate warming leads to decline in frequencies of melanic individuals in subarctic leaf beetle populations.

Intraspecific diversity buffers populations from deleterious impacts of environmental change. Nevertheless, the consequences of climate warming for phenotypic and genetic diversity within populations and species remain poorly understood. The goal of our study was to explore among-year variations in the phenotypic structure of populations and their relationships with climate variability and population dynamics. We analysed multiyear (1992-2018) data on colour morph frequencies within populations of the leaf beetle, Chrysomela lapponica, from multiple sites in the Kola Peninsula (northwestern Russia). We observed a strong decline in the proportion of dark (melanic) morphs among overwintered beetles during the study period; this decline was consistent across all study sites. Using model selection procedures, we explained declines in the dark morph of overwintered beetles by increases in minimum spring (May-June) daily temperatures. Other climatic characteristics, pollution load, and beetle population density were unrelated to variation in colour morph frequencies. Among newly emerged beetles (August), dark morph frequencies also decreased with an increase in average spring temperatures, but were unrelated to mean temperatures during the larval development period (July). These results suggest that the two-fold decline in dark morph frequencies during the past 26 years has been driven by the 2.5 °C increase in spring temperatures, most likely because dark males lose the mating advantages over light males that they obtain during cold springs. The continued loss of dark morphs and related decrease in within-population diversity may render leaf beetle populations more vulnerable to future environmental changes, in particular to those expressed in extreme weather fluctuations. Our study demonstrates that declines in within-population diversity are already underway in subarctic areas, and that these declines are likely driven by climate warming.