Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects.

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus' diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.

Amarillo-Suárez AR ，Fox CW 《OECOLOGIA》

Host-associated fitness variation in a seed beetle (Coleoptera: Bruchidae): evidence for local adaptation to a poor quality host.

The geographic distributions of many generalist herbivores differ from those of their host plants, such that they experience coarse-grained spatial variation in natural selection on characters influencing adaptation to host plants. Thus, populations differing in host use are expected to differ in their ability to survive and grow on these host plants. We examine host-associated variation in larval performance (survivorship, development time, and adult body weight) and oviposition preference, within and between two populations ofStator limbatus (Coleoptera: Bruchidae) that differ in the hosts available to them in nature. In one population,Acacia greggii (Fabaceae: Mimosoideae) andCercidium microphyllum (Fabaceae: Caesalpininoideae) are each abundant, while in the second population onlyC. floridum andC. microphyllum are present. In both populations, egg-to-adult survivorship was less than 50% onC. floridum, while survivorship was greater than 90% onA. greggii. Most of the mortality onC. floridum occurred as larvae were burrowing through the seed coat; very low mortality occurred during penetration of the seed coat ofA. greggii. Significant variation was present between populations, and among families (within populations), in survivorship and egg-to-adult development time onC. floridum; beetles restricted toCercidium in nature, without access toC. floridum, survived better and developed faster onC. floridum than beetles that had access toA. greggii. Large host effects on body size were detected for female offspring: females reared onA. greggii were larger than those reared onC. floridum, whereas male offspring wee approximately the same size regardless of rearing host. Trade-offs between performance onC. floridum andC. floridum were not detected in this experiment. Instead, our data indicate that development time and survivorship onC. floridum may be largely independent of development time and survivorship onA. greggii. Patterns of oviposition preference corresponded to the observed patterns of host suitability: in laboratory preference tests, beetles with access toA. greggii in nature tended to prefer this host more than beetles without access to this host in nature.

Fox CW ，Waddell KJ ，Mousseau TA 《-》

Selection on body size and sexual size dimorphism differs between host species in a seed-feeding beetle.

Sexual size dimorphism varies substantially among populations and species but we have little understanding of the sources of selection generating this variation. We used path analysis to study how oviposition host affects selection on body size in a seed-feeding beetle (Stator limbatus) in which males contribute large ejaculates (nuptial gifts) to females. Females use nutrients in these ejaculates for egg production. Male body size, which affects ejaculate size, affects female fecundity and is thus under fecundity selection similar in magnitude to the fecundity selection on female body size. We show that when eggs are laid on a host on which larval mortality is low (seeds of Acacia greggii) fecundity predicts fitness very well and fecundity selection is the major source of selection on both male and female adult size. In contrast, when eggs are laid on a host on which larval mortality is high (seeds of Parkinsonia florida) fecundity poorly predicts fitness such that fecundity selection is relaxed on both male and female size. However, because egg size affects larval mortality on this poor host (P. florida) there is selection on female size via the female size --> egg size --> fitness path; this selection via egg size offsets the reduction in fecundity selection on female, but not male, body size. Thus, differences in host suitability (due to differences in larval mortality) affect the relative importance of two sources of selection on adult body size; fecundity selection on both male and female body size is lower on the poor quality host (P. florida) relative to the high quality host (A. greggii) whereas selection on female body size via effects of egg size on offspring survival (body size --> egg size --> fitness) is greater on the poor quality host relative to the high quality host. Because selection via the egg size path affects only females the difference in larval survival between hosts shifts the relative magnitude of selection on female vs. male size. Researchers working on other study systems should be alerted to the possible importance of subtle, but consequential, indirect selection on their study organisms.

Fox CW ，Czesak ME 《JOURNAL OF EVOLUTIONARY BIOLOGY》

THE EVOLUTIONARY GENETICS OF AN ADAPTIVE MATERNAL EFFECT: EGG SIZE PLASTICITY IN A SEED BEETLE.

In many organisms, a female's environment provides a reliable indicator of the environmental conditions that her progeny will encounter. In such cases, maternal effects may evolve as mechanisms for transgenerational phenotypic plasticity whereby, in response to a predictive environmental cue, a mother can change the type of eggs that she makes or can program a developmental switch in her offspring, which produces offspring prepared for the environmental conditions predicted by the cue. One potentially common mechanism by which females manipulate the phenotype of their progeny is egg size plasticity, in which females vary egg size in response to environmental cues. We describe an experiment in which we quantify genetic variation in egg size and egg size plasticity in a seed beetle, Stator limbatus, and measure the genetic constraints on the evolution of egg size plasticity, quantified as the genetic correlation between the size of eggs laid across host plants. We found that genetic variation is present within populations for the size of eggs laid on seeds of two host plants (Acacia greggii and Cercidium floridum; h ranged between 0.217 and 0.908), and that the heritability of egg size differed between populations and hosts (higher on A. greggii than on C. floridum). We also found that the evolution of egg size plasticity (the maternal effect) is in part constrained by a high genetic correlation across host plants (r > 0.6). However, the cross-environment genetic correlation is less than 1.0, which indicates that the size of eggs laid on these two hosts can diverge in response to natural selection and that egg size plasticity is thus capable of evolving in response to natural selection.

Fox CW ，Czesak ME ，Mousseau TA ，Roff DA ... -  《-》

Phenotypic plasticity in a complex world: interactive effects of food and temperature on fitness components of a seed beetle.

Most studies of phenotypic plasticity investigate the effects of an individual environmental factor on organism phenotypes. However, organisms exist in an ecologically complex world where multiple environmental factors can interact to affect growth, development and life histories. Here, using a multifactorial experimental design, we examine the separate and interactive effects of two environmental factors, rearing host species (Vigna radiata, Vigna angularis and Vigna unguiculata) and temperature (20, 25, 30 and 35 degrees C), on growth and life history traits in two populations [Burkina Faso (BF) and South India (SI)] of the seed beetle, Callosobruchus maculatus. The two study populations of beetles responded differently to both rearing host and temperature. We also found a significant interaction between rearing host and temperature for body size, growth rate and female lifetime fecundity but not larval development time or larval survivorship. The interaction was most apparent for growth rate; the variance in growth rate among hosts increased with increasing temperature. However, the details of host differences differed between our two study populations; the degree to which V. unguiculata was a better host than V. angularis or V. radiata increased at higher temperatures for BF beetles, whereas the degree to which V. unguiculata was the worst host increased at higher temperatures for SI beetles. We also found that the heritabilities of body mass, growth rate and fecundity were similar among rearing hosts and temperatures, and that the cross-temperature genetic correlation was not affected by rearing host, suggesting that genetic architecture is generally stable across rearing conditions. The most important finding of our study is that multiple environmental factors can interact to affect organism growth, but the degree of interaction, and thus the degree of complexity of phenotypic plasticity, varies among traits and between populations.

Stillwell RC ，Wallin WG ，Hitchcock LJ ，Fox CW ... -  《OECOLOGIA》