Peter J. Mayhew

Adaptive patterns of host-plant selection by phytophagous insects

Host-plant selection by phytophagous insects is largely determined by adult insects choosing the developmental location of offspring. Knowledge of natural selection leads to theoretical predictions about how adult behaviour might respond to host quality, the abundance of host-plants, adult egg-load, age and available search time, density-dependence, and stochastic effects. Debates about the value of simple adaptive models can only be settled by repeated testing and reformulation. The theoretical basis of adaptive host-selection is quite strong, but several challenges remain. Models are lacking which are both general enough to be applicable to a wide range of species, and easy to test. The role of variability in plant abundance and other stochastic forces requires clarification. Empirically, good field studies of the effect of host-plants on insect fitness are rare, but without them little progress can be made. The assessment of host-preference also requires attention. Quantitative tests of theory are rare, probably because general models do not encompass enough relevant natural history for each particular species. However much anecdotal and qualitative evidence seems to reflect adaptive predictions. A challenge for the future is to assess the adaptive value of particular mechanisms of host-selection, and to relate these to the predictions made in simple adaptive models.

Herbivore host choice and optimal bad motherhood

When theory predicts which phenotypes are well adapted to a given environment, the data do not always match the predictions. Host-plant selection by herbivorous insects is one such example. Herbivorous insects often appear to make poor choices about where their offspring should develop. New evidence presented by Scheirs et al. suggests that adult insects can choose oviposition sites that enhance their own long-term fitness at the expense of their individual offspring. This suggests that herbivorous insects might be genuinely bad mothers, that host choice is nonetheless adaptive, and that theory needs to incorporate new assumptions about host effects on adult performance.

A long-term association between global temperature and biodiversity, origination and extinction in the fossil record.

The past relationship between global temperature and levels of biological diversity is of increasing concern due to anthropogenic climate warming. However, no consistent link between these variables has yet been demonstrated. We analysed the fossil record for the last 520 Myr against estimates of low latitude sea surface temperature for the same period. We found that global biodiversity (the richness of families and genera) is related to temperature and has been relatively low during warm ‘greenhouse’ phases, while during the same phases extinction and origination rates of taxonomic lineages have been relatively high. These findings are consistent for terrestrial and marine environments and are robust to a number of alternative assumptions and potential biases. Our results provide the first clear evidence that global climate may explain substantial variation in the fossil record in a simple and consistent manner. Our findings may have implications for extinction and biodiversity change under future climate warming.

Why are there so many insect species? Perspectives from fossils and phylogenies

Over half of all described species are insects, but until recently our understanding of the reasons for this diversity was based on very little macroevolutionary evidence. Here I summarize the hypotheses that have been posed, tests of these hypotheses and their results, and hence identify gaps in knowledge for future researchers to pursue. I focus on inferences from the following sources: (i) the fossil record, normally at family level, and (ii) insect phylogenies, sometimes combined with: (iii) the species richness of insect higher taxa, and (iv) current extinction risks.

Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression

Population genetic models have suggested that siblicide between the larvae of parasitoid wasps, once gained, can be lost only under stringent conditions, making transitions from solitary to gregarious development rare. However, phylogenetic studies suggest that gregarious development has evolved on numerous occasions, although the mechanisms are largely unknown. We report experiments, on two morphologically similar species of alysiine braconids, directed at an understanding of how gregarious development evolved in one subfamily. We compared the oviposition behaviour and development of Aphaereta genevensis and A. pallipes in the laboratory, on the host Drosophila virilis. Aphaereta genevensis usually lays a single egg in each host, and only a single wasp usually develops successfully even when several eggs are laid. However, A. pallipes often lays more than one egg in each host, and several offspring often complete development. Dissections of superparasitized hosts showed that this difference is accompanied by differences in larval behaviour: first-instar A. genevensis use their sharp mandibles to kill other parasitoid eggs or larvae in the same host. First-instar A. pallipes also have sharp mandibles, but do not attack conspecific larvae, suggesting that siblicide might have been lost by a simple change in larval behaviour. Aphaereta genevensis shows some features that may have helped select for reduction in larval aggression in the subfamily: a longer development time, multiple egg clutches and incomplete brood reduction. Aphaereta spp. show great promise as model systems for studying the evolution of siblicide. Copyright 1999 The Association for the Study of Animal Behaviour.

Biodiversity tracks temperature over time.

The geographic distribution of life on Earth supports a general pattern of increase in biodiversity with increasing temperature. However, some previous analyses of the 540-million-year Phanerozoic fossil record found a contrary relationship, with paleodiversity declining when the planet warms. These contradictory findings are hard to reconcile theoretically. We analyze marine invertebrate biodiversity patterns for the Phanerozoic Eon while controlling for sampling effort. This control appears to reverse the temporal association between temperature and biodiversity, such that taxonomic richness increases, not decreases, with temperature. Increasing temperatures also predict extinction and origination rates, alongside other abiotic and biotic predictor variables. These results undermine previous reports of a negative biodiversity-temperature relationship through time, which we attribute to paleontological sampling biases. Our findings suggest a convergence of global scale macroevolutionary and macroecological patterns for the biodiversity-temperature relationship.

Phylogenetic distribution of extant richness suggests metamorphosis is a key innovation driving diversification in insects.

Insects and their six-legged relatives (Hexapoda) comprise more than half of all described species and dominate terrestrial and freshwater ecosystems. Understanding the macroevolutionary processes generating this richness requires a historical perspective, but the fossil record of hexapods is patchy and incomplete. Dated molecular phylogenies provide an alternative perspective on divergence times and have been combined with birth-death models to infer patterns of diversification across a range of taxonomic groups. Here we generate a dated phylogeny of hexapod families, based on previously published sequence data and literature derived constraints, in order to identify the broad pattern of macroevolutionary changes responsible for the composition of the extant hexapod fauna. The most prominent increase in diversification identified is associated with the origin of complete metamorphosis, confirming this as a key innovation in promoting insect diversity. Subsequent reductions are recovered for several groups previously identified as having a higher fossil diversity during the Mesozoic. In addition, a number of recently derived taxa are found to have radiated following the development of flowering plant (angiosperm) floras during the mid-Cretaceous. These results reveal that the composition of the modern hexapod fauna is a product of a key developmental innovation, combined with multiple and varied evolutionary responses to environmental changes from the mid Cretaceous floral transition onward.

Shifts in hexapod diversification and what Haldane could have said

Data on species richness and taxon age are assembled for the extant hexapod orders (insects and their six–legged relatives). Coupled with estimates of phylogenetic relatedness, and simple statistical null models, these data are used to locate where, on the hexapod tree, significant changes in the rate of cladogenesis (speciation minus–extinction rate) have occurred. Significant differences are found between many successive pairs of sister taxa near the base of the hexapod tree, all of which are attributable to a shift in diversification rate after the origin of the Neoptera (insects with wing flexion) and before the origin of the Holometabola (insects with complete metamorphosis). No other shifts are identifiable amongst supraordinal taxa. Whilst the Coleoptera have probably diversified faster than either of their putative sister lineages, they do not stand out relative to other closely related clades. These results suggest that any Creator had a fondness for a much more inclusive clade than the Coleoptera, definitely as large as the Eumetabola (Holometabola plus bugs and their relatives), and possibly as large as the entire Neoptera. Simultaneous, hence probable causative events are discussed, of which the origin of wing flexion has been the focus of much attention.

Nonsiblicidal Behavior and the Evolution of Clutch Size in Bethylid Wasps

Parent‐offspring conflict over clutch size may lead to siblicidal behavior between juveniles. In parasitoid wasps, selection for siblicide in small broods is predicted to produce a dearth of gregarious broods with few eggs. Here we document the clutch size distribution in the Bethylidae, a large family of aculeate parasitoids. Small gregarious clutches are the most common. Further data suggest that the most common gregarious clutches in the parasitoid Hymenoptera as a whole contain only a few eggs. Across bethylid species, both clutch size and wasp size increase with host size. Within genera clutch size is more closely related to host size, but between genera or larger clades wasp size is more closely related to host size. The volume of the emerging wasp brood does not depend on whether a species lays single‐ or multiple‐egg clutches once host size is taken into account. These data suggest that clutch size in bethylid wasps is best described by traditional optimality models and that siblicide plays little role in this and possibly other families. We propose several ecological reasons for the rarity of siblicide in bethylids: ectoparasitism, idiobiosis, and a suite of characteristics associated with high within‐brood relatedness.

Small body size in an insect shifts development, prior to adult eclosion, towards early reproduction

Life-history theory has suggested that individual body size can strongly affect the allocation of resources to reproduction and away from other traits such as survival. In many insects, adults eclose with a proportion of their potential lifetime egg production that is already mature (the ovigeny index). We establish for the solitary parasitoid wasp Aphaereta genevensis that the ovigeny index decreases with adult body size, despite both initial egg load and potential lifetime fecundity increasing with body size. This outcome is predicted by adaptive models and is the first unequivocal intraspecific demonstration. Evidence suggests that a high ovigeny index carries a cost of reduced longevity in insects. Our results therefore contribute to the emerging evidence that small body size can favour a developmental shift in juveniles that favours early reproduction, but which has adverse late-life consequences. These findings are likely to have important implications for developmental biologists and population biologists.