Alternative Reproductive Phenotypes Research Articles

The Evolution of Alternative Buoyancy Mechanisms in Freshwater Fish Eggs

Alternative reproductive tactics (ARTs) are behavioural, morphological, and physiological traits associated with alternative reproductive phenotypes within a population or species. ARTs are widespread in nature, and are a particular feature of teleost fishes. However, few studies have examined egg buoyancy mechanisms in the context of the evolution of ARTs in freshwater fishes. In marine fishes, egg buoyancy is achieved chiefly through hydration. While the buoyancy of freshwater fish eggs has been suggested to be determined primarily through the presence of oil droplets, the majority (60%) of freshwater pelagic eggs do not possess an oil droplet. We applied a physical model of buoyancy to understand the contributions of oil droplets and hydration to the buoyancy of pelagic freshwater fish eggs. We further used phylogenetic regression to estimate the effect of the relative size of the perivitelline space, habitat and parental care on the occurrence of oil droplets, while controlling for non-independence among species due to phylogenetic relatedness. Our analysis demonstrates that the probability of oil droplets in freshwater pelagic eggs exhibits a significant negative relationship with the size of perivitelline space, which may reflect a trade-off relating to energy allocation in contrasting habitats. We also demonstrate a positive association between the probability of oil droplets and the provision of parental care and occupancy of lentic habitats. These findings indicates the evolution of contrasting buoyancy mechanisms as novel ARTs in freshwater fishes. A theoretical model in combination with empirical analysis indicate the evolution of novel ARTs in freshwater fishes as adaptive responses to flow conditions.

Cuticular and Dufour's Gland Chemistry Reflect Reproductive and Social State in the Facultatively Eusocial Sweat Bee Megalopta genalis (Hymenoptera: Halictidae).

Queen pheromones evolved independently in multiple eusocial insect lineages, in which they mediate reproductive conflict by inhibiting worker ovarian development. Although fundamentally important for reproductive division of labor - the hallmark of eusociality - their evolutionary origins are enigmatic. Here, we analyze cuticular and Dufour's gland chemistries across alternative social and reproductive phenotypes in Megalopta genalis bees (tribe Augochlorini, family Halictidae) that facultatively express simple eusociality. Reproductive bees have distinct overall glandular and cuticular chemical phenotypes compared with non-reproductive workers. On the cuticle, a likely site of signal transmission, reproductives are enriched for certain alkenes, most linear alkanes, and are heavily enriched for all methyl-branched alkanes. Chemicals belonging to these compound classes are known to function as fertility signals in other eusocial insect taxa. Some macrocyclic lactones, compounds that serve as queen pheromones in the other eusocial halictid tribe (Halictini), are also enriched among reproductives relative to workers. The intra-population facultative eusociality of M. genalis permits direct comparisons between individuals expressing alternative reproductive phenotypes - females that reproduce alone (solitary reproductives) and social queens - to highlight traits in the latter that may be important mediators of eusociality. Compared with solitary reproductives, the cuticular chemistries of queens are more strongly differentiated from those of workers, and furthermore are especially enriched for methyl-branched alkanes. Determining the pheromonal function(s) and information content of the candidate signaling compounds we identify will help illuminate the early evolutionary history of queen pheromones, chemical signals central to the organization of insect eusocial behavior.

Mate availability determines use of alternative reproductive phenotypes in hermaphrodites

Abstract In many species, individuals can employ alternative reproductive phenotypes, with profound consequences for individual fitness and population dynamics. This is particularly relevant for self-compatible hermaphrodites, which have exceptionally many reproductive options. Here we investigated the occurrence of reproductive phenotypes in the simultaneously hermaphroditic freshwater snail Radix balthica under experimentally simulated conditions of low versus moderate population density. We captured all mating behavior on camera and measured individual female lifetime reproductive success. We found every possible reproductive phenotype: (1) both male and female (i.e., truly hermaphroditic) reproduction, (2) purely female and (3) purely male reproduction, (4) male reproduction combined with self-fertilization and (5) female mating activity, (6) pure self-fertilization without mating and (7–8) two types of reproductive failure. Variation in alternative reproductive phenotypes was explained by mate availability (10.8%) and individual condition, approximated by a snail’s mean daily growth rate (17.5%). Increased mate availability resulted in a lower diversity of reproductive phenotypes, in particular increasing the frequency of true hermaphrodites. However, it lowered phenotype-specific fecundities and hence reduced the population growth rate. Snails in better condition were more likely to reproduce as true hermaphrodites or pure females, whereas low-condition snails tended to suffer reproductive failure. Overall, we show substantial variation in alternative reproductive phenotypes in a hermaphrodite, which is possibly in part maintained by fluctuations in population density and thus mate availability, and by variation in individual condition. We also provide evidence of an almost 2-fold increase in clutch size that can be ascribed specifically to mating as a female.

Relative costs and benefits of alternative reproductive phenotypes at different temperatures \u2013 genotype-by-environment interactions in a sexually selected trait

BackgroundThe maintenance of considerable genetic variation in sexually selected traits (SSTs) is puzzling given directional selection expected to act on these traits. A possible explanation is the existence of a genotype-by-environment (GxE) interaction for fitness, by which elaborate SSTs are favored in some environments but selected against in others. In the current study, we look for such interactions for fitness-related traits in the bulb mite, a male-dimorphic species with discontinuous expression of a heritable SST in the form of enlarged legs that are used as weapons.ResultsWe show that evolution at 18 °C resulted in populations with a higher prevalence of this SST compared to evolution at 24 °C. We further demonstrate that temperature modified male reproductive success in a way that was consistent with these changes. There was a genotype-by-environment interaction for reproductive success – at 18 °C the relative reproductive success of armored males competing with unarmored ones was higher than at the moderate temperature of 24 °C. However, male morph did not have interactive effects with temperature with respect to other life history traits (development time and longevity).ConclusionsA male genotype that is associated with the expression of a SST interacted with temperature in determining male reproductive success. This interaction caused an elaborate SST to evolve in different directions (more or less prevalent) depending on the thermal environment. The implication of this finding is that seasonal temperature fluctuations have the potential to maintain male polymorphism within populations. Furthermore, spatial heterogeneity in thermal conditions may cause differences among populations in SST selection. This could potentially cause selection against male immigrants from populations in different environments and thus strengthen barriers to gene flow.

Subfamily-dependent alternative reproductive strategies in worker honeybees.

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.

Female Mimicry by Sneaker Males Has a Transcriptomic Signature in Both the Brain and the Gonad in a Sex-Changing Fish.

Phenotypic plasticity represents an elegant adaptive response of individuals to a change in their environment. Bluehead wrasses (Thalassoma bifasciatum) exhibit astonishing sexual plasticity, including female-to-male sex change and discrete male morphs that differ strikingly in behavior, morphology, and gonadal investment. Using RNA-seq transcriptome profiling, we examined the genes and physiological pathways underlying flexible behavioral and gonadal differences among female, dominant (bourgeois) male, and female-mimic (sneaker) male blueheads. For the first time in any organism, we find that female mimicry by sneaker males has a transcriptional signature in both the brain and the gonad. Sneaker males shared striking similarity in neural gene expression with females, supporting the idea that males with alternative reproductive phenotypes have "female-like brains." Sneaker males also overexpressed neuroplasticity genes, suggesting that their opportunistic reproductive strategy requires a heightened capacity for neuroplasticity. Bourgeois males overexpressed genes associated with socio-sexual behaviors (e.g., isotocin), but also neuroprotective genes and biomarkers of oxidative stress and aging, indicating a hitherto unexplored cost to these males of attaining the reproductively privileged position at the top of the social hierarchy. Our novel comparison of testicular transcriptomes in a fish with male sexual polymorphism associates greater gonadal investment by sneaker males with overexpression of genes involved in cell proliferation and sperm quality control. We propose that morphological female-mimicry by sneaker male teleosts entails pervasive downregulation of androgenesis genes, consistent with low androgen production in males lacking well-developed secondary sexual characters.

The effects of paternal reproductive tactic and rearing environment on juvenile variation in growth as mediated through aggression and foraging behaviours of Chinook salmon (Oncorhynchus tshawytscha)

In species with indeterminate growth, differential growth rates can lead to animals adopting alternative reproductive tactics such as sneak–guard phenotypes, which is partially predicted by variation in growth during the juvenile life-history stage. To investigate sources of growth variation, we examined the independent and joint effects of paternal reproductive tactic (G) and rearing environment (E) on juvenile growth in Chinook salmon (Oncorhynchus tshawytscha), hypothesizing G and E effects are partially mediated through differences in behaviour such as aggressive interactions and resulting foraging behaviours. We created maternal half-sibling families with one-half of the female's eggs fertilized by the milt of a sneaker “jack” and the other half by a guarder “hooknose”. At the exogenous feeding stage, each split-clutch family was then divided again and reared in a rationed diet or growth-promotion diet environment for approximately 6 months, during which growth parameters were measured. Before saltwater transfer at 9 months of age, social interactions were observed in groups of six fish of various competitor origins. We found ration restricts growth rate and juvenile mass, and evidence of genetic effects on growth depensation, where jack-sired individuals grew less uniformly over time. These growth-related differences influenced an individual's level of aggression, with individuals raised on a restricted diet and those whose families experienced greatest growth being most aggressive. These individuals were more likely to feed than not and feed most often. Jack-sired individuals were additionally aggressive in the absence of food, and when raised on a rationed diet outcompeted others to feed most. These results show how individuals may achieve higher growth rates via intrinsic (G) or induced (E) aggressive behavioural phenotypes, and eventually attain the threshold body size necessary during the saltwater phase to precociously sexually mature and adopt alternative reproductive phenotypes.

Otolith morphology varies between populations, sexes and male alternative reproductive tactics in a vocal toadfish Porichthys notatus.

In this study, the morphology of sagittal otoliths of the plainfin midshipman fish Porichthys notatus was compared between populations, sexes and male alternative reproductive phenotypes (known as 'type I males or guarders' and 'type II males or sneakers'). Sagitta size increased with P. notatus size and changes in shape were also detected with increasing body size. Porichthys notatus sagittae begin as simple rounded structures, but then elongate as they grow and take on a more triangular and complex shape with several prominent notches and indentations along the dorsal and caudal edges. Moreover, the sagittae of the two geographically and genetically distinct populations of P. notatus (northern and southern) differed in shape. Porichthys notatus from the north possessed taller sagittae with deeper caudal indentations compared to P. notatus from the south. Sagitta shape also differed between females and males of the conventional guarder tactic. Furthermore, guarder males had smaller sagittae for their body size than did sneaker males or females. These differences in sagittal otolith morphology are discussed in relation to ecological and life history differences between the sexes and male tactics of this species. This is the first study to investigate teleost otolith morphology from the perspective of alternative reproductive tactics.

Experimental evolution reveals balancing selection underlying coexistence of alternative male reproductive phenotypes.

Heritable alternative reproductive phenotypes (ARPs), which differ in traits associated with competition for mates, occur across taxa. If polymorphism in the genes underlying ARPs is maintained by balancing selection, selection should return ARP proportions to their equilibrium if that equilibrium is perturbed. Here, we used an experimental evolution approach to directly test this prediction in male Rhizoglyphus robini, in which two heritable morphs occur: armored fighters and more female-like, benign scramblers. Using selection lines nearly fixed for male morph, we constructed replicate populations consisting of 50% or 94% fighters, and allowed them to evolve for 14 generations in two types of environment: simple or spatially complex. We found that in both types of populations, the proportion of fighters converged on values within a narrow range of 0.70-0.83, although the rate of convergence was slower in the complex environment. Our results thus demonstrate balancing selection acting on polymorphism(s) underlying ARPs.

The influence of hybridization with domesticated conspecifics on alternative reproductive phenotypes in male Atlantic salmon in multiple temperature regimes

Alternative reproductive phenotypes represent adaptive life-history responses to local environments. Hybridization with domesticated conspecifics exposed to selection against one of the phenotypes could affect the plasticity and incidence of alternative reproductive phenotypes within wild populations, potentially influencing individual fitness and population viability. We addressed this hypothesis by undertaking a common-garden experiment on Atlantic salmon (Salmo salar), a species in which males mature either as large, migratory anadromous individuals or as small, generally nonmigratory parr. Comparing one wild population and two domesticated–wild hybrids (F1, wild backcrosses), we evaluated the incidence of parr maturity at three different temperatures. Parr maturation probability exhibited a significant quadratic relationship with body mass. Early maturation was absent in the coldest temperature treatment. Body-size maturation thresholds were higher in the warmest temperature treatment relative to the intermediate temperature treatment, resulting in a similar incidence of maturation in both treatments despite increased growth in the warmest temperature treatment. Although body-size thresholds for parr maturity did not differ between crosses, F1 hybrids and backcrosses exhibited a lower incidence of maturity relative to wild fish (4.8%, 9.3%, and 30.1%, respectively). Changes in the incidence of alternative maturation phenotypes resulting from temperature and domesticated–wild hybridization could have negative fitness consequences for wild populations.

Endocrine correlates of mate choice and promiscuity in females of a socially monogamous avian mating system with alternative male reproductive phenotypes

Abstract While our understanding of male reproductive strategies is informed by extensive investigations into endocrine mechanisms, the proximate mechanisms by which females compete for mates and adjust reproduction to social environment remains enigmatic. We set out to uncover endocrine correlates of mate choice, social environment, and reproductive investment in female red-backed fairy-wrens Malurus melanocephalus. In this socially monogamous, yet highly sexually promiscuous species, females experience discrete variation in the phenotype of their mates, which vary in both plumage signals and level of paternal care, and in the composition of their breeding groups, which consist of either the pair alone or with an additional cooperative auxiliary; female investment varies according to these social parameters. We found that androgen, estrogen, and glucorticoid levels varied with reproductive stage, with highest androgen and estrogen concentrations during nest construction and highest corticosterone concentrations during the pre-breeding stage. These stage-dependent patterns did not vary with male phenotype or auxiliary presence, though androgen levels during pre-breeding mate selection were lower in females obtaining red/black mates than those obtaining brown mates. We found no evidence that androgen, estrogen, or corticosterone levels during the fertile period were related to extra-pair young (EPY) frequency. This study demonstrates clear changes in steroid levels with reproductive stage, though it found little support for variation with social environment. We suggest hormonal responsiveness to social factors may be physiologically constrained in ways that are bypassed through exogenous hormone manipulations.

Neural Gene Expression Profiles and Androgen Levels Underlie Alternative Reproductive Tactics in the Ocellated Wrasse, Symphodus ocellatus

AbstractDiscrete variation in reproductive behavior and physiology is observed in diverse taxa. Although it is known that most within‐sex alternative reproductive tactics arise as a consequence of phenotypic plasticity, relatively little is known about differential neural gene expression among plastic alternative reproductive phenotypes. In the ocellated wrasse Symphodus ocellatus, males exhibit one of three alternative tactics (nesting, satellite, and sneaker) within a reproductive season, but switch tactics between years. Satellites and sneakers spawn parasitically in dominant (nesting) males' nests, but only nesting males provide parental care. Nesting and satellite males show transient cooperative defense of nests against sneakers. Here, we analyze circulating sex steroid hormone levels and neural gene expression profiles in these three male phenotypes and in females. 11‐ketotestosterone (but not testosterone) was highest in nesting males, while estradiol was highest in females. Brain transcriptomes of satellites and females were most similar to each other and intermediate to nesting and sneaker males. Sneakers showed more total expression differences, whereas nesting males showed higher magnitude expression differences. Our findings reveal the surprising extent to which neural gene expression patterns vary across reproductive tactics that vary in a number of social traits, including aggression, territoriality, and cooperation, providing important insights into the molecular mechanisms that may underlie variation in cooperative and reproductive behavior.

Does frequency-dependence determine male morph survival in the bulb mite Rhizoglyphus robini?

Alternative reproductive phenotypes (ARPs) represent discrete morphological variation within a single sex; as such ARPs are an excellent study system to investigate the maintenance of phenotypic variation. ARPs are traditionally modelled as a mixture of pure strategies or as a conditional strategy. Most male dimorphisms are controlled by a conditional strategy, where males develop into a particular phenotype as a result of their condition which allows them to reach a certain threshold. Individuals that are unable to reach the threshold of a conditional strategy are considered to 'make the best of a bad job'; however, these individuals can have their own fitness merits. Given these fitness merits, condition-dependent selection alone is not sufficient to maintain a conditionally determined male dimorphism and other mechanisms, most likely frequency-dependent selection, are required. We studied in an experiment, the male dimorphic bulb mite Rhizoglyphus robini-where males are fighters that can kill other males or benign scramblers-to assess the strength of frequency-dependent survival in a high and low-quality environment. We found that male survival was frequency-dependent in the high-quality environment but not the low-quality environment. In the high-quality environment the survival curves of the two morphs crossed but the direction of frequency-dependence was opposite to what theory predicts.

Complex response in size-related traits of the bulb mites (Rhizoglyphus robini) in elevated thermal conditions - an experimental evolution approach

Temperature is a key environmental factor affecting almost all aspects of life history in ectotherms. Theory predicts that they grow faster, reach smaller sizes and produce smaller offspring when temperature increases. In addition, temperature changes, through their effects on metabolism, may also influence the expression of alternative reproductive phenotypes (ARPs) in ectotherms. Although many studies have investigated the phenotypic plasticity of life history traits in relation to temperature change, little is known about how those traits and phenotypic plasticity may evolve together. In our study we subjected bulb mites (non-model, soil organisms that normally experience rather stable thermal conditions) to experimental evolution in two temperature treatments: control (24°C) and elevated (28°C). After 18 generations, we measured adult body size, egg size and development time of both treatments at control as well as at elevated temperatures (test temperatures). Thus, we were able to detect genetic changes (the effects of selection temperature) and environmental effects (the effects of test temperature). We also observed the ARP expression throughout the experimental evolution. Our results revealed quite complex patterns of life history in traits response to temperature. Mites developed faster and reached smaller sizes at increased temperature, but evolutionary responses to increased temperature were not always parallel to the observed phenotypic plasticity. Additionally, despite smaller body sizes, females laid larger eggs at higher temperature. This effect was more pronounced in animals evolving at elevated temperature. Evolution at increased temperature also affected ARP expression, with the proportion of armored fighters decreasing from generation to generation. We propose that this could be the consequence of temperature sensitivity of the cost-to-benefits ratio of expressing ARPs.

Condition-dependent signaling and adoption of mating tactics in an amphibian with energetic displays

Most alternative reproductive phenotypes are interpreted as alternative tactics within a conditional strategy: all individuals are predicted to choose among behavioral tactics based on some measure of their physiological condition or competitive status. The factors determining a male’s tactic at any particular time are generally unknown. Thus, most researchers have measured potential correlates of competitive ability (such as male body size) rather than directly measuring fighting ability, for example, in males adopting alternative mating tactics. In species in which sexual competition primarily involves production of acoustic signals, an individual’s choice of mating tactic may largely depend on physical characteristics, such as age, strength, or condition, which determine its ability to compete acoustically by producing attractive calls. Male green tree frogs (Hyla cinerea) often switch tactics (caller or satellite), but body size changes very little during the breeding season. I tested the hypothesis that mating-tactic switches are mediated via the effects of changing body condition on advertisement call characteristics. My field study shows that the switch between tactics is predicted by condition but not by size. Moreover, short-term changes in body weight result in condition-dependent changes in several properties of the advertisement call. The demonstration of condition-dependent advertisement calling and tactic adoption links a physical characteristic correlated with mating-tactic adoption with actual competitive status (calling performance). Vocal fatigue may constrain males to produce relatively unattractive advertisement calls, thus increasing the potential fitness payoffs associated with adoption of the satellite tactic.

Fitness trade‐offs and the maintenance of alternative male morphs in the bulb mite (Rhizoglyphus robini)

Alternative reproductive phenotypes (ARPs) occur across a wide range of taxa. Most ARPs are conditionally expressed in response to a cue, for example body size, that reliably correlates with the status of the environment: individuals below the (body size) threshold then develop into one morph, and individuals above the threshold develop into the alternative morph. The environmental threshold model provides a theoretical framework to understand the evolution and maintenance of such ARPs, yet no study has examined the underlying fitness functions that are necessary to realize this. Here, we empirically examined fitness functions for the two male morphs of the bulb mite (Rhizoglyphus robini). Fitness functions were derived in relation to male size for solitary males and in relation to female size under competition. In both cases, the fitness functions of the two morphs intersected, and the resulting fitness trade-offs may play a role in the maintenance of this male dimorphism. We furthermore found that competition was strongest between males of the same morph, suggesting that fitness trade-off in relation to male size may persist under competition. Our results are a first step towards unravelling fitness functions of ARPs that are environmentally cued threshold traits, which is essential for understanding their maintenance and in explaining the response to selection against alternative morphs.

Enhanced growth reduces precocial male maturation in Atlantic salmon

Summary1. Understanding the proximate and ultimate mechanisms shaping the expression of alternative reproductive phenotypes is a fundamental question in life‐history evolution. Precocial maturation in fishes, one such alternative phenotype, has been thought to reflect rapid growth and/or energy accumulation; however, mechanistically linking these specific traits to discrete life‐history patterns is complex and poorly understood.2. Here, we use growth hormone (GH) transgenic Atlantic salmon to elucidate the effects of intrinsically fast growth on precocial male maturation as parr (freshwater life stage). Despite facilitating growth to sizes typical of mature wild‐type parr, transgenesis did not influence maturation in the first year of life. In the second year, the number of maturing transgenic parr was only half that of non‐transgenic individuals.3. By manipulating intrinsic growth and controlling for both environment and genetic background, this study provides direct empirical evidence suggesting that the physiological mechanisms promoting growth do not play a causative role in precocial male maturation in fishes.4. In addition, this study provides the first empirical data on the relative incidence of precocial male maturation in GH transgenic and non‐transgenic Atlantic salmon and, therefore, provides valuable information for the ecological risk assessment process.

Genome-wide analysis of alternative reproductive phenotypes in honeybee workers

A defining feature of social insects is the reproductive division of labour, in which workers usually forego all reproduction to help their mother queen to reproduce. However, little is known about the molecular basis of this spectacular form of altruism. Here, we compared gene expression patterns between nonreproductive, altruistic workers and reproductive, non-altruistic workers in queenless honeybee colonies using a whole-genome microarray analysis. Our results demonstrate massive differences in gene expression patterns between these two sets of workers, with a total of 1292 genes being differentially expressed. In nonreproductive workers, genes associated with energy metabolism and respiration, flight and foraging behaviour, detection of visible light, flight and heart muscle contraction and synaptic transmission were overexpressed relative to reproductive workers. This implies they probably had a higher whole-body energy metabolism and activity rate and were most likely actively foraging, whereas same-aged reproductive workers were not. This pattern is predicted from evolutionary theory, given that reproductive workers should be less willing to compromise their reproductive futures by carrying out high-risk tasks such as foraging or other energetically expensive tasks. By contrast, reproductive workers mainly overexpressed oogenesis-related genes compared to nonreproductive ones. With respect to key switches for ovary activation, several genes involved in steroid biosynthesis were upregulated in reproductive workers, as well as genes known to respond to queen and brood pheromones, genes involved in TOR and insulin signalling pathways and genes located within quantitative trait loci associated with reproductive capacity in honeybees. Overall, our results provide unique insight into the molecular mechanisms underlying alternative reproductive phenotypes in honeybee workers.

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.

Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren

Understanding how pre- and postcopulatory sexually selected traits covary can provide insight into the evolution of male ornamentation and female mate choice. In this study, we examined ejaculate quality and investment in testicular tissue in relation to plumage colour and social status in the genetically promiscuous red-backed fairy-wren, Malurus melanocephalus. In this species, males exhibit one of three alternative reproductive phenotypes during the breeding season: males can breed in red and black plumage, breed in brown plumage, or act as brown-plumed, nonbreeding auxiliaries. We found that red/ black breeders invested more heavily in spermatogenic tissue, had larger sperm reserves, and tended to have greater numbers of sperm in ejaculate samples, when compared to brown breeders and auxiliaries. Within red/black breeders, plumage redness and saturation (i.e. long wavelength hue and increased red chroma) were negatively correlated with ejaculate sample sperm density. In addition, ejaculate motility appeared to be related to variation in plumage coloration such that, overall, males with less elaborate ornamentation showed greater ejaculate quality. These results suggest that pre- and postcopulatory traits negatively covary in red/black plumed red-backed fairy-wrens and indicate a possible trade-off between investment in plumage ornaments and investment in ejaculates.