Sexual dimorphism in immunity across animals: a meta-analysis.

In animals, sex differences in immunity are proposed to shape variation in infection prevalence and intensity among individuals in a population, with females typically expected to exhibit superior immunity due to life-history trade-offs. We performed a systematic meta-analysis to investigate the magnitude and direction of sex differences in immunity and to identify factors that shape sex-biased immunocompetence. In addition to considering taxonomic and methodological effects as moderators, we assessed age-related effects, which are predicted to occur if sex differences in immunity are due to sex-specific resource allocation trade-offs with reproduction. In a meta-analysis of 584 effects from 124 studies, we found that females exhibit a significantly stronger immune response than do males, but the effect size is relatively small, and became non-significant after controlling for phylogeny. Female-biased immunity was more pronounced in adult than immature animals. More recently published studies did not report significantly smaller effect sizes. Among taxonomic and methodological subsets of the data, some of the largest effect sizes were in insects, further supporting previous suggestions that testosterone is not the only potential driver of sex differences in immunity. Our findings challenge the notion of pervasive biases towards female-biased immunity and the role of testosterone in driving these differences.

Multiple cues influence multiple traits in the phenotypically plastic melanization of the cabbage white butterfly.

Phenotypic plasticity, or the ability of organisms to produce different phenotypes depending upon environmental factors, may be adaptive in varying environments. However, because environments differ in many ways and organisms consist of many traits perfect phenotype-environment matches are unlikely. Studies that investigate multiple interacting environmental factors and the plastic responses of multiple traits should increase our understanding of the limits of adaptive plasticity. We experimentally examined the effects of variation in temperature and photoperiod on the seasonally plastic, and likely adaptive, melanization of a temperate butterfly, Pieris rapae. Although several melanin-based traits changed in response to temperature and photoperiodic variation, these traits tended to fall into two 'trait groups' consisting of traits covarying positively. However, these two trait groups responded to environmental factors, particularly temperature, in independent and sometimes opposing ways, with one increasing and the other decreasing in melanization with increased temperature. In some cases, plastic responses were complex and non-linear. Furthermore, when temperature and photoperiod were manipulated orthogonally, we sometimes detected interactive effects on melanization. These complex responses to two environmental cues may reflect sub-optimal responses or may occur if the two cues together provide more reliable information about future conditions than would either cue alone. Our results highlight the limits of studies of phenotypic plasticity that consider only single environmental factors and limit treatments to just two levels.

Eyespots deflect predator attack increasing fitness and promoting the evolution of phenotypic plasticity.

Some eyespots are thought to deflect attack away from the vulnerable body, yet there is limited empirical evidence for this function and its adaptive advantage. Here, we demonstrate the conspicuous ventral hindwing eyespots found on Bicyclus anynana butterflies protect against invertebrate predators, specifically praying mantids. Wet season (WS) butterflies with larger, brighter eyespots were easier for mantids to detect, but more difficult to capture compared to dry season (DS) butterflies with small, dull eyespots. Mantids attacked the wing eyespots of WS butterflies more frequently resulting in greater butterfly survival and reproductive success. With a reciprocal eyespot transplant, we demonstrated the fitness benefits of eyespots were independent of butterfly behaviour. Regardless of whether the butterfly was WS or DS, large marginal eyespots pasted on the hindwings increased butterfly survival and successful oviposition during predation encounters. In previous studies, DS B. anynana experienced delayed detection by vertebrate predators, but both forms suffered low survival once detected. Our results suggest predator abundance, identity and phenology may all be important selective forces for B. anynana. Thus, reciprocal selection between invertebrate and vertebrate predators across seasons may contribute to the evolution of the B. anynana polyphenism.

Resource-based trade-offs and the adaptive significance of seasonal plasticity in butterfly wing melanism.

Phenotypic plasticity is the ability of an organism to alter its phenotype in response to environmental cues. This can be adaptive if the cues are reliable predictors of impending conditions and the alterations enhance the organism's ability to capitalize on those conditions. However, since traits do not exist in isolation but as part of larger interdependent systems of traits (phenotypic integration), trade-offs between correlated plastic traits can make phenotypic plasticity non- or maladaptive. We examine this problem in the seasonally plastic wing melanism of a pierid (Order Lepidoptera, Family Pieridae) butterfly, Pieris rapae L. Several wing pattern traits are more melanized in colder than in warmer seasons, resulting in effective thermoregulation through solar absorption. However, other wing pattern traits, the spots, are less melanized during colder seasons than in warmer seasons. Although spot plasticity may be adaptive, reduced melanism of these spots could also be explained by resource-based trade-offs. Theory predicts that traits involved in resource-based trade-offs will be positively correlated when variation among individuals in resource acquisition is greater than variation among individuals in resource allocation strategies, and negatively correlated when variation in allocation is greater than variation in acquisition. Using data from both field studies and laboratory studies that manipulate dietary tyrosine, a melanin precursor, we show that when allocation to thermoregulatory melanism (ventral hindwing, and basal dorsal fore- and hindwing "shading") varies substantially this trait is negatively correlated with spot melanism. However, when there is less variation in allocation to thermoregulatory melanism we find these traits to be positively correlated; these findings are consistent with the resource-based trade-off hypothesis, which may provide a non- or maladaptive hypothesis to explain spot plasticity. We also show that increased dietary tyrosine results in increased spot melanism under some conditions, supporting the more general idea that melanism may involve resource-based costs.

Immune defense and host life history.

Recent interest has focused on immune response in an evolutionary context, with particular attention to disease resistance as a life-history trait, subject to trade-offs against other traits such as reproductive effort. Immune defense has several characteristics that complicate this approach, however; for example, because of the risk of autoimmunity, optimal immune defense is not necessarily maximum immune defense. Two important types of cost associated with immunity in the context of life history are resource costs, those related to the allocation of essential but limited resources, such as energy or nutrients, and option costs, those paid not in the currency of resources but in functional or structural components of the organism. Resource and option costs are likely to apply to different aspects of resistance. Recent investigations into possible trade-offs between reproductive effort, particularly sexual displays, and immunity have suggested interesting functional links between the two. Although all organisms balance the costs of immune defense against the requirements of reproduction, this balance works out differently for males than it does for females, creating sex differences in immune response that in turn are related to ecological factors such as the mating system. We conclude that immune response is indeed costly and that future work would do well to include invertebrates, which have sometimes been neglected in studies of the ecology of immune defense.

Spalt expression and the development of melanic color patterns in pierid butterflies.

BACKGROUND: Little is currently known about wing pattern development in the butterfly family Pieridae, which consists mostly of black melanized elements on white or yellow/orange backgrounds. A single transcription factor, Spalt (Sal), has been previously associated with the development of some pattern elements in Pieris rapae, but it is unclear to what extent Sal is associated with patterns in other pierid species. RESULTS: We use immunohistochemistry targeting Sal proteins across several pierids and show that Sal is associated with dense patches of melanization across species but is not associated with vein-melanization or diffuse melanization on the wing. In addition, Sal is expressed along cross-veins and wing compartment midlines that do not develop melanization. Male and female P. rapae spots are sexually dimorphic in size and this dimorphism is also present in the domains of Sal expression. Finally, by disrupting cells positioned in the center of the anterior black spots of P. rapae, before and during the time of Sal expression, spot size was reduced. CONCLUSIONS: Our results suggest, but do not conclusively show, that pierid spots may develop in a manner similar to that of nymphalid eyespots, that is, containing a group of signaling cells at the center of the pattern responsible for the differentiation of the complete spot, and that spots and eyespots share at least one signal-response gene in common, the transcription factor Sal. We propose that focal differentiation and focal signaling mechanisms evolved prior to the split of the nymphalid and pierid lineages.

Phenotypic plasticity: molecular mechanisms and adaptive significance.

Phenotypic plasticity can be broadly defined as the ability of one genotype to produce more than one phenotype when exposed to different environments, as the modification of developmental events by the environment, or as the ability of an individual organism to alter its phenotype in response to changes in environmental conditions. Not surprisingly, the study of phenotypic plasticity is innately interdisciplinary and encompasses aspects of behavior, development, ecology, evolution, genetics, genomics, and multiple physiological systems at various levels of biological organization. From an ecological and evolutionary perspective, phenotypic plasticity may be a powerful means of adaptation and dramatic examples of phenotypic plasticity include predator avoidance, insect wing polymorphisms, the timing of metamorphosis in amphibians, osmoregulation in fishes, and alternative reproductive tactics in male vertebrates. From a human health perspective, documented examples of plasticity most commonly include the results of exercise, training, and/or dieting on human morphology and physiology. Regardless of the discipline, phenotypic plasticity has increasingly become the target of a plethora of investigations with the methodological approaches utilized ranging from the molecular to whole organsimal. In this article, we provide a brief historical outlook on phenotypic plasticity; examine its potential adaptive significance; emphasize recent molecular approaches that provide novel insight into underlying mechanisms, and highlight examples in fishes and insects. Finally, we highlight examples of phenotypic plasticity from a human health perspective and underscore the use of mouse models as a powerful tool in understanding the genetic architecture of phenotypic plasticity.