Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen

Parasite-mediated selection is potentially of great importance in modulating genetic diversity. Genetic variation for resistance, the fuel for natural selection, appears to be common in host-parasite interactions, but responses to selection are rarely observed. In the present study, we tested whether environmental variation could mediate infection and determine evolutionary outcomes. Temperature was shown to dramatically alter the potential for parasite-mediated selection in two independent laboratory infection experiments at four temperatures. The bacterial parasite, Pasteuria ramosa, was extremely virulent at 20 degrees C and 25 degrees C, sterilizing its host, Daphnia magna, so that females often never produced a single brood. However, at 10 degrees C and 15 degrees C, the host-parasite interaction was much more benign, as nearly all females produced broods before becoming sterile. This association between virulence and temperature alone could stabilize coexistence and lead to the maintenance of diversity, because it would weaken parasite-mediated selection during parts of the season. Additionally, highly significant genotype-by-environment interactions were found, with changes in clone rank order for infection rates at different temperatures. Our results clearly show that the outcome of parasite-mediated selection in this system is strongly context dependent.     

The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics

We model the evolution of reaction norms focusing on three aspects: frequency-dependent selection arising from resource competition, maintenance and production costs of phenotypic plasticity, and three characteristics of environmental heterogeneity (frequency of environments, their intrinsic carrying capacity and the sensitivity to phenotypic maladaptation in these environments). We show that (i) reaction norms evolve so as to trade adaptation for acquiring resources against cost avoidance; (ii) maintenance costs cause reaction norms to better adapt to frequent rather than to infrequent environments, whereas production costs do not; and (iii) evolved reaction norms confer better adaptation to environments with low rather than with high intrinsic carrying capacity. The two previous findings contradict earlier theoretical results and originate from two previously unexplored features that are included in our model. First, production costs of phenotypic plasticity are only incurred when a given phenotype is actually produced. Therefore, they are proportional to the frequency of environments, and these frequencies thus affect the selection pressure to avoid costs just as much as the selection pressure to improve adaptation. This prevents the frequency of environments from affecting the evolving reaction norm. Secondly, our model describes the evolution of plasticity for a phenotype determining an individual's capability to acquire resources, and thus its realized carrying capacity. When individuals are distributed randomly across environments, they cannot avoid experiencing environments with intrinsically low carrying capacity. As selection pressures arising from the need to improve adaptation are stronger under such extreme conditions than under mild ones, better adaptation to environments with low rather than with high intrinsic carrying capacity results.     

Phenotypic plasticity of abdominal pigmentation in Drosophila kikkawai: multiple interactions between a major gene, sex, abdomen segment and growth temperature

Drosophila kikkawai is known to be polymorphic for a single autosomal locus controlling abdomen pigmentation in females. Two strains homozygous at this locus (Abdomen pigmentation, Abp) were established from a polymorphic Indian population: one was homozygous (DD) for the dark allele, the other (LL) for the light allele. A Mendelian analysis of crosses at 25°C confirmed the occurrence of a major locus, with dominance of the D allele. Phenotypic variation of pigmentation according to growth temperature was then analyzed in DD and LL male and female flies, and in reciprocal F1. A slight difference was found between reciprocal F1 females from a dark mother were darker but not at all temperatures. In females, the D allele exhibited an antero‐posterior gradient of increasing expression from segment 27, with dominance over L and an increased expression at low temperatures. In males, abdomen pigmentation was uniformly light in segments 25, the D allele being repressed by the sex genotype. In segment 6, the D allele was expressed but only at low temperatures, and was either recessive to L or codominant. Phenotypic plasticity that is, amount of change induced by different growth temperatures, was variable according to genotype and segment. It always corresponded to a darkening of the fly at lower temperatures, but was generally much less than in D. melanogaster. In D. kikkawai, climatic adaptation might occur more by changing the frequency of the D allele than by phenotypic plasticity. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genetic variance of sexually selected traits in waxmoths: maintenance by genotype x environment interaction

When traits experience directional selection, such as that imposed by sexual selection, their genetic variance is expected to diminish. Nonetheless, theory and findings from sexual selection predict and demonstrate that male traits favored by female choice retain substantial amounts of additive genetic variance. We explored this dilemma through an ecological genetic approach and focused on the potential contributions of genotype x environment interaction (GEI) to maintenance of additive genetic variance for male signal characters in the lesser waxmoth, Achroia grisella (Lepidoptera: Pyralidae). We artificially selected genetic variants for two male signal characters, signal rate (SR) and peak amplitude (PA), that influence female attraction and then examined the phenotypic plasticity of these variants (high- and low-SR and high- and low-PA lines) under a range of environmental conditions expected in natural populations. Our split-family breeding experiments indicated that two signal characters, SR and PA, and several developmental characters in both high- and low-SR and high- and low-PA lines displayed considerable phenotypic plasticity among the environments tested. Moreover, strong GEIs leading to crossover between high- and low-SR lines were found for SR and developmental period. Therefore, neither high- nor low-SR genetic variants would achieve maximum attractiveness and fitness in every environment, and those variants producing unattractive signals with low SRs under normal conditions may remain in populations provided that gene flow across environments or generation overlap are sufficiently high. We speculate that the phenotypic plasticity for SR and developmental period is adaptive in A. grisella populations experiencing a range of temperature and density conditions. Females mating with attractive (high-SR) males may be assured of obtaining good genes because these males sire offspring that develop more rapidly and a crossover for developmental period may parallel that for SR. Such parallel crossovers may be expected wherever good-genes sexual selection mechanisms operate.     

Phenotypic plasticity in female mate choice behavior is mediated by an interaction of direct and indirect genetic effects in Drosophila melanogaster

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.     

Sex-specific genotype-by-environment interactions for cuticular hydrocarbon expression in decorated crickets, Gryllodes sigillatus: implications for the evolution of signal reliability

Phenotypic traits that convey information about individual identity or quality are important in animal social interactions, and the degree to which such traits are influenced by environmental variation can have profound effects on the reliability of these cues. Using inbred genetic lines of the decorated cricket, Gryllodes sigillatus, we manipulated diet quality to test how the cuticular hydrocarbon (CHC) profiles of males and females respond across two different nutritional rearing environments. There were significant differences between lines in the CHC profiles of females, but the effect of diet was not quite statistically significant. There was no significant genotype-by-environment interaction (GEI), suggesting that environmental effects on phenotypic variation in female CHCs are independent of genotype. There was, however, a significant effect of GEI for males, with changes in both signal quantity and content, suggesting that environmental effects on phenotypic expression of male CHCs are dependent on genotype. The differential response of male and female CHC expression to variation in the nutritional environment suggests that these chemical cues may be under sex-specific selection for signal reliability. Female CHCs show the characteristics of reliable cues of identity: high genetic variability, low condition dependence and a high degree of genetic determination. This supports earlier work showing that female CHCs are used in self-recognition to identify previous mates and facilitate polyandry. In contrast, male CHCs show the characteristics of reliable cues of quality: condition dependence and a relatively higher degree of environmental determination. This suggests that male CHCs are likely to function as cues of underlying quality during mate choice and/or male dominance interactions.     

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post‐copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high‐ and low‐temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P₂), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P₁). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre‐ejaculatory environment and sexual selection in the post‐ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post‐copulatory sexual selection.     

Rapid temporal change in the expression and age-related information content of a sexually selected trait

The expression of sexual signals is often phenotypically plastic and also evolves rapidly. Few studies have considered the possibility that proximate determination -- the pathway between genes and trait expression -- may also be subject to both phenotypic plasticity and evolutionary change. We examined long-term patterns in size, condition- and age-dependence, repeatability and heritability of forehead patch size, a sexually selected plumage trait in male collared flycatchers. We also estimated survival and sexual selection on the phenotypic value of the trait. Forehead patch size linearly declined during the 15 years, probably due to the significantly negative survival selection. In addition, the expression of genetic variation for the ornament apparently underwent an age-limited change, which implies a change in the information content of the signal to receivers. The persistent lack of condition-dependence makes phenotypic plasticity an unlikely explanation to our results. This raises the possibility of a microevolutionary change of both expression and proximate determination during the study period.     

Artificial selection on the shape of reaction norms for eyespot size in the butterfly Bicyclus anynana: direct and correlated responses

The tropical butterfly Bicyclus anynana shows phenotypic plasticity in its ventral wing pattern as an adaptive response to wet‐dry seasonality. Wet season form individuals have large eyespots, whereas individuals of the dry season generation have small eyespots. In the laboratory these forms can be obtained by rearing larvae at high and low temperatures, respectively. To study the extent to which the shape of the nearly linear reaction norms for eyespot size can be changed we applied four generations of sib selection by rearing full‐sib families across three temperatures. In addition, we measured ecdysteroid titres shortly after pupation in the final generation. Although phenotypic variation in shape was present initially, the experiment yielded lines with reaction norms with similar shapes but different elevations. High, positive genetic correlation across temperatures can explain this lack of response. Differences in ecdysteroid titres did not readily relate to differences in eyespot size.     

Genotype x environment interaction for male attractiveness in an acoustic moth: evidence for plasticity and canalization

The lek paradox arises when choosy females deplete the genetic variance for male display traits from a population, yet substantial additive genetic variation (V_A) in male traits persists. Thus, the lek paradox can be more generally stated as one of the most fundamental evolutionary questions: What maintains genetic variation in natural populations? One solution to this problem may be found in the condition‐dependent nature of many sexually selected traits. Genotype × environment (G × E) interactions can maintain V_A under conditions of environmental heterogeneity provided certain restrictions are met, although antagonistic pleiotropy has also been proposed as a mechanism. Here, we provide evidence for G × E interactions and against the role of antagonistic pleiotropy in the maintenance of V_A for sexually selected traits. Using inbred lines of the lesser waxmoth Achroia grisella, we measured V_A for song attractiveness, condition and development rate under different competitive environments and found that genotypes differed in their plasticity. We argue that variation persists in natural populations because G × E interactions prevent any one variant from producing the optimal phenotype across all environments.     

Sensitive periods during the development and expression of vertebrate sexual signals: A systematic review

Many sexually selected traits exhibit phenotypic plasticity. Despite a growing appreciation for the ecological context in which sexual selection occurs, and for the role of plasticity in shaping traits associated with local adaptation and divergence, there is an important gap in knowledge about the onset and duration of plasticity in sexual trait expression. Integrating this temporal dimension of plasticity into models of sexual selection informs our understanding of the information conveyed by sexual traits and our predictions related to trait evolution, and is critical in this time of unprecedented and rapid environmental change. We conducted a systematic review of 869 studies to ask how trait modalities (e.g., visual and chemical) relate to the onset and duration of plasticity in vertebrate sexual signals. We show that this literature is dominated by studies of coloration in birds and fish, and most studies take place during the breeding season. Where possible, we integrate results across studies to link physiology of specific trait modalities with the life stage (e.g., juvenile, breeding, or nonbreeding) during which plasticity occurs in well‐studied traits. Limitations of our review included a lack of replication in our dataset, which precluded formal analysis. We argue that the timing of trait plasticity, in addition to environmental context, is critical for determining whether and how various communication signals are associated with ecological context, because plasticity may be ongoing or occur at only one point in an individual''s lifetime, and determining a fixed trajectory of trait expression. We advocate for careful consideration of the onset and duration of plasticity when analyzing how environmental variation affects sexual trait expression and associated evolutionary outcomes.     

Male mate choice and the potential for complex mating dynamics in the tree lizard (Urosaurus ornatus)

A growing body of literature is recognizing that males may also play a role in the mating process by behaving non‐randomly toward potential female mates during courtship. In numerous species, discrete color polymorphisms in males are inferred to represent alternative mating tactics, which often correspond with concomitant asymmetries in ecology and behavior. In terms of their mating behavior, these ecological outcomes of a color polymorphism should affect a morph's likelihood and frequency of encountering females in a population, possibly favoring the evolution of morph‐specific mating preferences. Knowledge of how male morphs contribute to a species’ overall mating dynamics will improve our understanding of how sexual selection shapes phenotypic diversity in color polymorphic systems. We conducted a mate choice experiment to evaluate the extent and morph specificity of non‐random mating preferences by male ornate tree lizards, Urosaurus ornatus. We observed the behavior of blue and yellow males in an experimental arena in response to a choice between an orange or yellow female. We found that blue males preferred yellow females over orange females, and although yellow males visited females more often than blue males overall, their attention was not morph‐specific. Given male morph differences in choosiness, and their differences in social dominance, we conclude that female throat color may be partly under sexual selection in U. ornatus. However, a lack of concordance between male and female mating preferences (drawn from an earlier study) suggests that overall mating dynamics may serve to maintain, rather than enhance, color morph differences in this species.     

Crest evolution in newts: implications for reconstruction methods, sexual selection, phenotypic plasticity and the origin of novelties

The dorsal crest of newts (Salamandridae) is a novel, phenotypically plastic, sexually selected trait that may evolve in association with complex courtship behaviours. We estimated a near-comprehensive, time-calibrated phylogeny for salamandrids and analysed the evolution of their crests and display behaviour. Different models give conflicting reconstructions for crest evolution, showing that likelihood can estimate incorrect ancestral states with strong statistical support. The best-fitting model suggests that crests evolved once and were lost repeatedly, supporting the hypothesis that sexually selected traits may be frequently lost. We demonstrate the correlated evolution of crests and courtship behaviour and show that species with larger numbers of crest-related traits have larger repertoires of behaviours. We also show that phenotypically plastic morphological traits can be maintained over long macroevolutionary timescales (～25-48 Myr). Finally, we use salamandrids to address how novel structures may arise, and support a model involving the expansion and subdivision of pre-existing structures.     

Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna

A resurrection ecology reconstruction of 14 morphological, life history and behavioural traits revealed that a natural Daphnia magna population rapidly tracked changes in fish predation by integrating phenotypic plasticity and widespread evolutionary changes both in mean trait values and in trait plasticity. Increased fish predation mainly generated rapid adaptive evolution of plasticity (especially in the presence of maladaptive ancestral plasticity) resulting in an important change in the magnitude and direction of the multivariate reaction norm. Subsequent relaxation of the fish predation pressure resulted in reversed phenotypic plasticity and mainly caused evolution of the trait means towards the ancestral pre‐fish means. Relaxation from fish predation did, however, not result in a complete reversal to the ancestral fishless multivariate phenotype. Our study emphasises that the study population rapidly tracked environmental changes through a mosaic of plasticity, evolution of trait means and evolution of plasticity to generate integrated phenotypic changes in multiple traits.     

Dietary stress increases the total opportunity for sexual selection and modifies selection on condition‐dependent traits

Although it is often expected that adverse environmental conditions depress the expression of condition‐dependent sexually selected traits, the full consequences of environmental change for the action of sexual selection, in terms of the opportunity for total sexual selection and patterns of phenotypic selection, are unknown. Here we show that dietary stress in guppies, Poecilia reticulata, reduces the expression of several sexually selected traits and increases the opportunity for total sexual selection (standardized variance in reproductive success) in males. Furthermore, our results show that dietary stress modulates the relative importance of precopulatory (mating success) and postcopulatory (relative fertilization success) sexual selection, and that the form of multivariate sexual selection (linear vs. nonlinear) depends on dietary regime. Overall, our results are consistent with a pattern of heightened directional selection on condition‐dependent sexually selected traits under environmental stress, and underscore the importance of sexual selection in shaping adaptation in a changing world.     

Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development

Recent work on a diverse array of echinoderm species has demonstrated, as is true in amphibians, that thyroid hormone (TH) accelerates development to metamorphosis. Interestingly, the feeding larvae of several species of sea urchins seem to obtain TH through their diet of planktonic algae (exogenous source), whereas nonfeeding larvae of the sand dollar Peronella japonica produce TH themselves (endogenous source). Here we examine the effects of TH (thyroxine) and a TH synthesis inhibitor (thiourea) on the development of Dendraster excentricus, a sand dollar with a feeding larva. We report reduced larval skeleton lengths and more rapid development of the juvenile rudiment in the exogenous TH treatments when compared to controls. Also, larvae treated with exogenous TH reached metamorphic competence faster at a significantly reduced juvenile size, representing the greatest reduction in juvenile size ever reported for an echinoid species with feeding larvae. These effects of TH on D. excentricus larval development are strikingly similar to the phenotypically plastic response of D. excentricus larvae reared under high food conditions. We hypothesize that exogenous (algae-derived) TH is the plasticity cue in echinoid larvae, and that the larvae use ingested TH levels as an indicator for larval nutrition, ultimately signaling the attainment of metamorphic competence. Furthermore, our experiments with the TH synthesis inhibitor thiourea indicate that D. excentricus larvae can produce some TH endogenously. Endogenous TH production might, therefore, be a shared feature among sand dollars, facilitating the evolution of nonfeeding larval development in that group. Mounting evidence on the effects of thyroid hormones in echinoderm development suggests life-history models need to incorporate metamorphic hormone effects and the evolution of metamorphic hormone production.     

Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments

Adaptive phenotypic plasticity evolves when cues reliably predict fitness consequences of life‐history decisions, whereas bet hedging evolves when environments are unpredictable. These modes of response should be jointly expressed, because environmental variance is composed of both predictable and unpredictable components. However, little attention has been paid to the joint expression of plasticity and bet hedging. Here, I examine the simultaneous expression of plasticity in germination rate and two potential bet‐hedging traits – germination fraction and within‐season diversification in timing of germination – in seeds from multiple seed families of five geographically distant populations of Lobelia inflata (L.) subjected to a thermal gradient. Populations differ in germination plasticity to temperature, in total germination fraction and in the expression of potential diversification in the timing of germination. The observation of a negative partial correlation between the expression of plasticity and germination variance (potential diversification), and a positive correlation between plasticity and germination fraction is suggestive of a trade‐off between modes of response to environmental variance. If the observed correlations are indicative of those between adaptive plasticity and bet hedging, we expect an optimal balance to exist and differ among populations. I discuss the challenges involved in testing whether the balance between plasticity and bet hedging depends on the relative predictability of environmental variance.     

Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.