The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Special Issue: Ecology of Sex and Sexual Communication in Insects.

Sexual reproduction places constraints on both the place and time in which individuals can reproduce, as the sperm and ova need to meet in a certain location within a specific time frame for successful reproduction [...].

Diversity in warning coloration: selective paradox or the norm?

Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency-dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator-prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once-paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.

Do the benefits of polyandry scale with outbreeding?

There have been many potential explanations put forward as to why polyandry often persists despite the multiple costs it can inflict on females. One such explanation is avoidance of costs associated with mating with genetically incompatible males. Genetic incompatibility can be thought of as a spectrum from individuals that are genetically too similar (inbreeding) to those that are too dissimilar (outbreeding or hybridization). Here we look for evidence that the level of outbreeding influences the benefits of polyandry in the seed bug Lygaeus equestris. Our system allows us to test for benefits of polyandry at levels of genetic similarity ranging from full siblings to heterospecifics, both in terms of egg production and hatching success. We found that while outbreeding level appeared to have no effect on fitness for intraspecific matings, and polyandry did not appear to result in any increase in fertility or fecundity, hybridization with a closely related species, Lygaeus simulans, carried considerable fitness costs. However, these costs could be rescued with a single mating to a conspecific. Thus, polyandry may be beneficial in populations that co-occur with closely related species and where there is reproductive interference. However, within-species genetic incompatibility is unlikely to be the driving force behind polyandry in this species. Furthermore, the mechanism underlying this rescue of fertility remains unclear as manipulation of male cuticular hydrocarbon profile, a possible mechanism by which females can assess male identity, had no effect on female offspring production.

Experimental reduction of intromittent organ length reduces male reproductive success in a bug.

It is now clear in many species that male and female genital evolution has been shaped by sexual selection. However, it has historically been difficult to confirm correlations between morphology and fitness, as genital traits are complex and manipulation tends to impair function significantly. In this study, we investigate the functional morphology of the elongate male intromittent organ (or processus) of the seed bug Lygaeus simulans, in two ways. We first use micro-computed tomography (micro-CT) and flash-freezing to reconstruct in high resolution the interaction between the male intromittent organ and the female internal reproductive anatomy during mating. We successfully trace the path of the male processus inside the female reproductive tract. We then confirm that male processus length influences sperm transfer by experimental ablation and show that males with shortened processi have significantly reduced post-copulatory reproductive success. Importantly, male insemination function is not affected by this manipulation per se. We thus present rare, direct experimental evidence that an internal genital trait functions to increase reproductive success and show that, with appropriate staining, micro-CT is an excellent tool for investigating the functional morphology of insect genitalia during copulation.

The evolutionary ecology of the Lygaeidae.

The Lygaeidae (sensu lato) are a highly successful family of true bugs found worldwide, yet many aspects of their ecology and evolution remain obscure or unknown. While a few species have attracted considerable attention as model species for the study of insect physiology, it is only relatively recently that biologists have begun to explore aspects of their behavior, life history evolution, and patterns of intra- and interspecific ecological interactions across more species. As a result though, a range of new phenotypes and opportunities for addressing current questions in evolutionary ecology has been uncovered. For example, researchers have revealed hitherto unexpectedly rich patterns of bacterial symbiosis, begun to explore the evolutionary function of the family's complex genitalia, and also found evidence of parthenogenesis. Here we review our current understanding of the biology and ecology of the group as a whole, focusing on several of the best-studied characteristics of the group, including aposematism (i.e., the evolution of warning coloration), chemical communication, sexual selection (especially, postcopulatory sexual selection), sexual conflict, and patterns of host-endosymbiont coevolution. Importantly, many of these aspects of lygaeid biology are likely to interact, offering new avenues for research, for instance into how the evolution of aposematism influences sexual selection. With the growing availability of genomic tools for previously "non-model" organisms, combined with the relative ease of keeping many of the polyphagous species in the laboratory, we argue that these bugs offer many opportunities for behavioral and evolutionary ecologists.

Variation in social and sexual behaviour in four species of aposematic seed bugs (Hemiptera: Lygaeidae): the role of toxic and non-toxic food.

Understanding variation in social behaviour both within and among species continues to be a challenge. Evolutionary or ecological theory typically predicts the optimal behaviour for an animal under a given set of circumstances, yet the real world presents much greater variation in behaviour than predicted. This variation is apparent in many social and sexual interactions, including mate choice, and has led to a renewed focus on individual variation in behaviour. Here we explore within and among species variation in social behaviour in four species of aposematic seed bug (Lygaeidae: Hemiptera). These species are Müllerian mimics, with characteristic warning colouration advertising their chemical toxicity. We examine the role of diet in generating variation in two key behaviours: social aggregation of nymphs and mate choice. We test how behaviour varies with exposure to either milkweed (a source of defensive compounds) or sunflower (that provides no defence). We show that although the four species vary in their food preferences, and diet influences their life-history (as highlighted by body size), social aggregation and mate choice is relatively unaffected by diet. We discuss our findings in terms of the evolution of aposematism, the importance of automimicry, and the role of diet in generating behavioural variation.