Genic capture and the genetic basis of sexually selected traits in the zebra finch

Abstract The lek paradox, in which female choice erodes genetic variation in male sexually selected traits, is a fundamental issue in sexual selection. If females gain only genetic benefits from preferentially having their ova fertilized by males with particular traits, what maintains variation in these traits? Under strong directional selection mediated through mate choice, the alleles for beneficial male traits are expected to go to fixation and exhibit little variation. A theoretical solution to the lek paradox is the genic capture hypothesis which states that: costly male traits subject to female choice are condition dependent, that male condition is dependent on genes at many loci and exhibits additive genetic variance, and that positive genetic correlations exist between sexually selected traits and condition. Using a captive population of the zebra finch Taeniopygia guttata, we tested two key predictions from this model: (1) that genetic variance exists in beak color which is a sexually selected trait, but also in condition and immune function, and (2) that positive genetic correlations exist between condition and beak color, and between beak color, condition, and immune function. Genetic parameters were estimated from a large breeding experiment involving 81 sires, 972 offspring, a pedigree of 1526 individuals, using the animal model. We employed the following index of body condition: residuals from a log‐log plot of body mass on tarsus length following a standardized and extended period of exercise, in which residual mass is known to reflect fat and protein reserves. Our results were broadly consistent with the genic capture hypothesis because we found (1) additive genetic variation in beak color and immune function and condition, and (2) positive genetic correlations between condition and beak color, and between condition, beak color, and several assays of immune responsiveness. However, both of these results need qualification. In the first case we identified an important general problem in estimating the coefficient of additive genetic variance (CV_A) in body condition. In the second case, although most of the genetic correlations were positive as predicted, only some were statistically significant, possibly due to our relatively small sample sizes, because genetic correlations typically have large standard errors and therefore require very large samples to be statistically significant. The statistically significant, positive genetic correlations included those between beak color and immune function (response to tetanus), and between immune function (response to tetanus) and condition, both of which indicate that females gain good genes from mating with males in good condition and/or with a redder beak color. We discuss the implications of our results for devising more rigorous but pragmatic tests of the genic capture hypothesis.     

Effects of larval crowding on quantitative variation for development time and viability in Drosophila melanogaster

Competition between individuals belonging to the same species is a universal feature of natural populations and is the process underpinning organismal adaptation. Despite its importance, still comparatively little is known about the genetic variation responsible for competitive traits. Here, we measured the phenotypic variation and quantitative genetics parameters for two fitness‐related traits—egg‐to‐adult viability and development time—across a panel of Drosophila strains under varying larval densities. Both traits exhibited substantial genetic variation at all larval densities, as well as significant genotype‐by‐environment interactions (GEIs). GEI was attributable to changes in the rank order of reaction norms for both traits, and additionally to differences in the between‐line variance for development time. The coefficient of genetic variation increased under stress conditions for development time, while it was higher at both high and low densities for viability. While development time also correlated negatively with fitness at high larval densities—meaning that fast developers have high fitness—there was no correlation with fitness at low density. This result suggests that GEI may be a common feature of fitness‐related genetic variation and, further, that trait values under noncompetitive conditions could be poor indicators of individual fitness. The latter point could have significant implications for animal and plant breeding programs, as well as for conservation genetics.     

Genic capture and resolving the lek paradox

The genic capture hypothesis offers a resolution to the question of how genetic variation in male sexually selected traits is maintained in the face of strong female preferences. The hypothesis is that male display traits are costly to produce and hence depend upon overall condition, which itself is dependent upon genes at many loci. Few attempts have been made to test the assumptions and predictions of the genic capture hypothesis rigorously and, in particular, little attention has been paid to determining the genetic basis of condition. Such tests are crucial to our understanding of the maintenance of genetic variation and in the evaluation of recent models that propose a role for sexual selection in the maintenance of sex. Here, we review approaches to testing the link between genetically determined condition and levels of sexual trait expression and consider the probable importance of deleterious mutations.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

On the evolution of heightened condition dependence of male sexual displays

The maintenance of genetic variation in male sexual display traits in the face of strong directional sexual selection from female preferences is an ongoing evolutionary conundrum. Condition dependence and the genic capture hypothesis are often cited as theoretical resolutions to this problem, yet little is known about the ability of condition dependence itself to evolve. We set out to test how a suite of cuticular hydrocarbons (CHCs) used in sexual displays are affected by adult diet and the potential for any condition-dependent response to evolve in a laboratory-adapted population of the Australian fruit fly Drosophila serrata. We performed a dietary manipulation within a half-sib breeding design, raising adult males either with or without access to live yeast, a manipulation that had previously shown strong effects on female fitness. Diet had strong phenotypic effects, with males from the different diets producing different CHC blends. The blend of CHCs under sexual selection showed a degree of elevated condition dependence. Regardless of the heightened sensitivity of favoured CHC blends to diet and the presence of genetic variance for the traits, we were unable to detect any genetic variance in the reaction norms for the male dietary response. Our results suggest that there is limited opportunity for males to evolve further condition dependence in response to yeast availability in this population.     

Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles

In Tribolium flour beetles and other organisms, individuals migrate between heterogeneous environments where they often encounter markedly different nutritional conditions. Under these circumstances, theory suggests that genotype-by-environment interactions (GEI) may be important in facilitating adaptation to new environments and maintaining genetic variation for male traits subject to directional selection. Here, we used a nested half-sib breeding design with Tribolium castaneum to partition the separate and joint effects of male genotype and nutritional environment on phenotypic variation in a comprehensive suite of life-history traits, reproductive performance measures across three sequential sexual selection episodes, and fitness. When male genotypes were tested across three nutritional environments, considerable phenotypic plasticity was found for male mating and insemination success, longevity and traits related to larval development. Our results also revealed significant additive genetic variation for male mating rate, sperm offence ability (P(2)), longevity and total fitness and for several traits reflecting both larval and adult resource use. In addition, we found evidence supporting GEI for sperm defence ability (P(1)), adult longevity and larval development; thus, no single male genotype outperforms others in every nutritional environment. These results provide insight into the potential roles of phenotypic plasticity and GEI in facilitating Tribolium adaptation to new environments in ecological and evolutionary time.     

An Experimental Test of the Relationship between Genetic Variation and Environmental Variation in Tribolium Flour Beetles

The hypothesis that a component of genetic variation for polygenic fitness traits is maintained by environmental heterogeneity was tested using an experimental system involving two species of flour beetles, Tribolium castaneum and T. confusum. Replicated populations of each species from a number of environmental treatments were analyzed for various fitness components following almost 60 generations of natural selection. Environmental differences consisted of flours of cereals commonly invaded by natural populations of these insects.—Tests for adaptation to environments were based on experiments in which populations were reared factorially on each flour, such that population treatment x flour interactions could be detected. Measurements were made of survival, growth rate, larval weight, pupal weight, developmental time, fecundity of individuals at low density and fecundity and cannibalism at high density in both fresh and conditioned media.—Flour differences were found to have significant effects on most traits. Evidence for significant genetic variation and significant genotype x environment interaction was also found. However, no evidence could be found to support the hypothesis that genetic variation was maintained by environmental heterogeneity in food resources. The absence of adaptation to the experimental treatments despite the presence of genetic variation in fitness components suggests that pleiotropy may assume an important role in determining net fitness values of polygenes.     

Quantitative genetics of adult behavioral response and larval physiological tolerance to permethrin in diamondback moth (Lepidoptera: Plutellidae)

We investigated the genetic basis of adult behavioral response and larval physiological tolerance to permethrin within two diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), populations from Wooster and Celeryville, OH, with different average levels of larval tolerance. The adult behavioral response was measured as oviposition site preference and was investigated using full-sib design and parent-offspring regression. Additive genetic variance (0.134 +/- 0.02) and the heritability (h2 = 0.31 +/- 0.08) for the behavioral response was significant for the Celeryville population, suggesting that in this population, a high proportion of phenotypic variation for adult behavioral response to permethrin was heritable genetic variation. The larval physiological response was measured with a topical application bioassay and was investigated using a half-sib design. Significant additive genetic variances and heritabilities for physiological tolerance to permethrin were detected in both populations. The genetic correlation between adult behavioral response and larval physiological tolerance to permethrin were negative, but significant only in the Celeryville population; indicating that adults from this population that are more behaviorally responsive produced offspring that are more susceptible to permethrin. Our findings have implications for the evolution and management of insecticide resistance in the diamondback moth. The adult behavioral response can lower the exposure of larvae to the insecticide, lowering selection pressure for physiological resistance in larvae. Furthermore, to the extent that the adult behavioral response increases fitness, it can indirectly select for larval susceptibility because of the negative correlation between the two traits.     

Density‐dependent natural selection in Drosophila: correlations between feeding rate,development time and viability

We have previously hypothesized that density‐dependent natural selection is responsible for a genetic polymorphism in crowded cultures of Drosophila. This genetic polymorphism entails two alternative phenotypes for dealing with crowded Drosophila larval cultures. The first phenotype is associated with rapid development, fast larval feeding rates but reduced absolute viability, especially in the presence of nitrogenous wastes like ammonia. The second phenotype has associated with it the opposite set of traits, slow development, slow feeding rates and higher viability. We suggested that these traits are associated due to genetic correlations and that an important selective agent in crowded larval cultures was high levels of ammonia. To test this hypothesis we have examined viability and larval feeding rates in populations kept at low larval densities but selected directly for (i) rapid egg‐to‐adult development, (ii) tolerance of ammonia in the larval environment and (iii) tolerance of urea in the larval environment. Consistent with our hypothesis we found that (i) larvae selected for rapid development exhibited increased feeding rates, and decreased viability in food laced with ammonia or urea relative to controls, and (ii) larvae selected to tolerate either ammonia or urea in their larval environment show reduced feeding rates but elevated survival in toxin‐laced food relative to controls. It would appear that development time and larval feeding rate are important characters for larvae adapting to crowded cultures. The correlated fitness effects of these characters provide important insights into the nature of density‐dependent natural selection.     

Integrating large‐scale geographic patterns in flight morphology,flight characteristics and sexual selection in a range‐expanding damselfly

While geographic trait variation along environmental clines is widespread, associated patterns in sexual selection remain largely unexplored. Geographic patterns in sexual selection may be expected if 1) phenotypes vary geographically and sexual selection is dependent on the local phenotypes in the population, and if 2) sexual selection is influenced by geographically structured environmental conditions. We quantified geographic variation in flight‐related traits and flight performance in mated and unmated males and tested for geographic variation in sexual selection on these traits in the poleward range‐expanding damselfly Coenagrion scitulum across a set of eleven core and edge populations ordered along thermal gradients in the larval and in the adult stage. We found little support for trait differentiation between core and edge populations, instead we found considerable geographic trait variation along the larval and adult thermal gradients. As expected under time constraints, body mass decreased with shorter larval growth seasons. Lower temperatures during the adult flight period were associated with a higher body mass, a higher flight speed and a higher fat content; these traits likely evolved to buffer flight ability at suboptimal temperatures and to optimize starvation resistance. Across the large geographic scale, we found a consistent higher flight duration in mated males. Instead, sexual selection for higher fat content was stronger in populations with lower adult flight temperatures and sexual selection for lower body mass acted only in edge populations. Our results indicate sexual selection on flight performance to be consistent over a large geographic scale and this despite the clear geographic patterns in sexual selection on the underlying morphological traits. Our results highlight that to fully understand the fitness implications of geographically changing trait patterns, researchers should consider the entire phenotype–performance–fitness axis and incorporate effects of geographically structured life‐stage specific environmental conditions on this axis.     

Interpreting Geographic Variation in Life-History Traits

The geographic variation in the length of the larval periodand the size at metamorphosis of the wood frog,Rana sylvatica,is examined for populations in the tundra of Canada, the mountainsof Virginia, and the lowlands of Maryland. We argue that theobserved differences in developmental plasticity, heriisbilitiesand genetic covariances of traits among localities result fromdifferential selection pressures in each environment, and arerelated to the physiological constraints inherent in developmentand to the degree of compromise between the timing and sizeat metamorphosis allowed in each environment. In Maryland populationsfitness has been maximized by evolutionary changes in size alone;body size in this population is canalized, has low heritabilityand is highly correlated with juvenile survival relative todevelopmental time. In Canada, minimum developmental time yieldsmaximum fitness; the length of the larval period in this populationis canalized and genetically monomorphic relative to body size.In contrast, fitness in the Virginia populations has been determinedby correlated and pleiotropic effects of genes on both developmentaltime and larval body size, and both traits are equally canalized,affect juvenile survivorship equally and display moderate heritabilities.These results stress the importance of interpreting variationin life-history traits relative to constraints inherent in developmentand those imposed by the environment. Heritability and survivorshipdata support the general notion that fitness traits should havelow levels of additive genetic variation, but also suggest thatantagonistic pleiotropy may act to preserve genetic variationin fitness traits under simultaneous selection, and cautionagainst inferring evolutionary importance of individual traitswithout considering the possible presence of pleiotropy.     

Evidence of reduced individual heterogeneity in adult survival of long‐lived species

The canalization hypothesis postulates that the rate at which trait variation generates variation in the average individual fitness in a population determines how buffered traits are against environmental and genetic factors. The ranking of a species on the slow‐fast continuum – the covariation among life‐history traits describing species‐specific life cycles along a gradient going from a long life, slow maturity, and low annual reproductive output, to a short life, fast maturity, and high annual reproductive output – strongly correlates with the relative fitness impact of a given amount of variation in adult survival. Under the canalization hypothesis, long‐lived species are thus expected to display less individual heterogeneity in survival at the onset of adulthood, when reproductive values peak, than short‐lived species. We tested this life‐history prediction by analysing long‐term time series of individual‐based data in nine species of birds and mammals using capture‐recapture models. We found that individual heterogeneity in survival was higher in species with short‐generation time (< 3 years) than in species with long generation time (> 4 years). Our findings provide the first piece of empirical evidence for the canalization hypothesis at the individual level from the wild.     

Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Low inbreeding depression in a sexual trait in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

The genic capture hypothesis implies that the expression of sexual ornaments largely depends on genes affecting resource acquisition and use. The ornaments should thus show high degree of directional dominance typical of life-history traits, and consequently, they should be severely affected by inbreeding. Here we investigated the effect of inbreeding on a sexual ornament (male eyespan) in stalk-eyed fly, Teleopsis dalmanni. For comparison, we also measured inbreeding depression in non-sexual morphological traits: female eyespan as well as wing and thorax lengths in both sexes. Both eyespan, and other morphological traits we measured, showed significant inbreeding depression. In accord with predictions of genic capture hypothesis, male eyespan did decrease under inbreeding significantly more than female eyespan. However, the decline in male eyespan was fully explained by overall decline in body length. Moreover, the magnitude of inbreeding depression in male eyespan was considerably lower than that typically observed for life-histories; in fact, it fitted within the range typically characterizing morphological traits. We therefore conclude that our results provide weak support for genic capture hypothesis.     

Genetic variation and a fitness tradeoff in the tolerance of gray treefrog (Hyla versicolor) tadpoles to the insecticide carbaryl

One of the major unanswered questions in the study of global amphibian declines is why only some species or populations suffer declines. A possible explanation is that species and populations vary in the genetic basis of their tolerance to environmental stress such as chemical contamination. The presence of genetic variation in tolerance to chemicals and in fitness traits of amphibians is essential for persistence of species populations through survival and successful reproduction in contaminated environments. We tested for the presence of genetic variation in the tolerance of amphibian larvae to the insecticide carbaryl using gray treefrog tadpoles (Hyla versicolor). We also assessed whether tolerance of tadpoles is negatively associated with larval performance traits directly related to adult fitness, thereby providing a test of the "cost of tolerance" hypothesis. Our results demonstrate significant variation in tolerance of tadpoles to the insecticide carbaryl within a single population of the gray treefrog, Hyla versicolor. Our half-sibship design indicates that variation among sires explains a significant amount of the variation in chemical tolerance thereby suggesting a heritability genetic basis. Our results also indicate the presence of a fitness tradeoff with tolerance to the chemical carbaryl being negatively correlated, or traded off, with survival of tadpoles reared in the field in the absence of the chemical. Knowledge of genetic tradeoffs with chemical tolerance under realistic environmental conditions will be important for predicting the rate of adaptation and potential for persistence of species. Finally, the partitioning of environmental and genetic variation in tolerance to chemicals is critical to identifying which species are most susceptible, the amount of genetic variance present, the potential for adaptation to contaminants, and the presence of fitness tradeoffs. Such information is necessary to clearly understand the persistence of populations, and ultimately, the processes leading to species declines.     

A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the pacific tree frog, Hyla regilla

Metamorphosis is assumed to be beneficial because it can break developmental links between traits in the different phases of a complex life-cycle and thereby allow larval and adult phases to adapt independently. I tested the prediction that correlations between the larval and adult phases are smaller than within stages. I estimated phenotypic and additive genetic variances and correlations for tadpole swimming speed, frog jump distance, body size, and larval period in a single population of the Pacific tree frog, Hyla regilla. These traits are known or reasonably assumed to be important for survival in this and other anuran species from temporary ponds. Only the three size variables were affected by sire identity. Heritabilities for locomotor performance, larval period, and size-independent performance were low (0.00-0.23) and not significant. Body size measurements showed somewhat higher and statistically significant heritabilities (0.24-0.34). Most traits were phenotypically correlated. On average, phenotypic correlations were larger between phases than within phases (0.41 vs. 0.28). Genetic correlations involving body-size traits were positive and large, and average within- and between-phase genetic correlation coefficients were identical (0.81). These results do not support the adaptive decoupling hypothesis, and they indicate that a paucity of additive genetic variation is a likely constraint on the evolution of traits measured for this population.     

Antagonistic, stage-specific selection on defensive chemical sequestration in a toxic butterfly

Larvae of the pipevine swallowtail ( Battus philenor ) sequester toxic alkaloids called aristolochic acids from their Aristolochia host plants, rendering both larvae and adults chemically defended against most predators. Using a chemically controlled artificial diet, we observed substantial among-family variation in sequestration ability and larval developmental rate in a population occurring in central Texas. Early instar larvae from families that sequester greater amounts of aristolochic acid showed increased survivorship in a field experiment in which cohorts from each family were exposed to natural predators, whereas among-family variation in growth rate did not predict survivorship. Conversely, the aristolochic acid content of adult butterflies was negatively correlated with adult fat content, a fitness correlate. Sequestration ability positively affects the probability of larval survivorship, but at the cost of adult fat content. The costs and benefits of aristolochic acid sequestration vary during the course of the butterfly's development, and these antagonistic selection pressures may explain why variation in sequestration ability persists in wild populations.     

What is wrong with absolute individual fitness?

One of the most basic facts about evolution is that fitness is a relative concept. It does not matter how well an organism survives and reproduces, only that it does so better than other organisms bearing alternative traits. Nevertheless, many evolutionary arguments are framed in terms of absolute individual fitness. The absolute fitness criterion (AFC) can be justified in terms of relative fitness only given certain assumptions that are frequently violated in nature. In particular, interactions must occur in groups that are randomly formed and phenotypic variation among groups must be tightly coupled to genetic variation. Complicating the genotype-phenotype relationship can cause phenotypic variation among groups to become nonrandom, even when the groups are randomly formed, favoring traits that do not maximize absolute individual fitness. Complex genotype-phenotype relationships and complex population structures require explicit models of evolutionary change based on relative fitness differences within and among groups.     

Sex, mutation and fitness: asymmetric costs and routes to recovery through compensatory evolution

A wild-type population of Drosophila melanogaster was used to assess the impact of a known deleterious mutation, nub(1), when it had (1) evolved for up to 180 generations with the mutation or (2) recently had the same mutant allele introgressed into it. Relative to this benchmark, we observed much stronger initial fitness depression in males (-74%) than in females (-38%) and also relatively greater fitness recovery by evolved males (+55%) than females (+17%). Experimental assays revealed amelioration in both juvenile and adult fitness and suggested that the greater relative recovery of male fitness was from gains through sexual selection. These evolutionary changes in male fertility depended on pairing with their coevolved mates for both mate choice and post-copulatory components of sexual selection. Without replication at the population level, these results are used to motivate a general hypothesis rather than definitively test it: Differences in reproductive optima may generally skew mutational effects towards the more strongly sexually-selected sex due to genic capture and condition dependence.