Combining genetic variation and phenotypic plasticity in tradeoff modelling

Tradeoffs lead to antagonistic relationships between phenotypic traits and are thought to be determined both genetically and environmentally. We present here an allocation model that distinguishes between the genetic and environmental components of variation in resource allocation. In this model we introduced plasticity of resource allocation which was considered to be an adaptive response to environmental variations. The results show that resource allocation plasticity is a key parameter for the existence of environmental (i.e. inter environments and intra genotype) correlations and is therefore necessary to detect environment-induced tradeoffs. We also investigated the impact of the resource allocation plasticity and other factors on genetic (i.e. inter genotypes) correlations. Our results show that resource allocation plasticity induces a masking effect of tradeoffs when studying genetic correlations and increases the masking effect of resource variation by making apparent correlations positive when negative correlations are expected. In addition, by simulating different sources of resource acquisition variation, we demonstrated that resource variation might have different effects on correlations according to the experimental design and the studied biological material. Further development of this model may be used to investigate the theoretical implications of tradeoffs in evolutionary biology and to improve design and interpretation of experimental studies.     

Analytic and simulation models predicting positive genetic correlations between traits linked by trade-offs

Summary Using a two-loci multiplicative model of resource allocation, we show how the existence of several levels of resource allocation may affect the sign of the genetic correlations between traits linked by trade-offs. Positive genetic correlations between components of fitness affected by genetic trade-offs may result from different amounts of genetic variability at the pleiotropic loci determining the allocation of resources. Thus positive genetic correlations may be obtained in the absence both of environmental variation and of differences between individuals in resource acquisition. Nevertheless, positive correlations between all components of fitness at the same time cannot be obtained without variability in the acquisition of resources.     

Genetic polymorphism and trade-offs in the early life-history strategy of the Pacific oyster, Crassostrea gigas (Thunberg, 1795): a quantitative genetic study

We investigated genetic variability and genetic correlations in early life-history traits of Crassostrea gigas. Larval survival, larval development rate, size at settlement and metamorphosis success were found to be substantially heritable, whereas larval growth rate and juvenile traits were not. We identified a strong positive genetic correlation between larval development rate and size at settlement, and argue that selection could optimize both age and size at settlement. However, trade-offs, resulting in costs of metamorphosing early and large, were suggested by negative genetic correlations or covariances between larval development rate/size at settlement and both metamorphosis success and juvenile survival. Moreover, size advantage at settlement disappeared with time during the juvenile stage. Finally, we observed no genetic correlations between larval and juvenile stages, implying genetic independence of life-history traits between life-stages. We suggest two possible scenarios for the maintenance of genetic polymorphism in the early life-history strategy of C. gigas.     

Life-history evolution in Anodonta piscinalis (Mollusca,Pelecypoda)

Summary The correlations between certain life-history parameters (reproductive effort, reproductive life-span, age of first reproduction, general growth index, variation in juvenile survival, availability of resources) were studied in 13 populations of the mussel Anodonta piscinalis in south-western Finland in 1975 and 1976Reproductive life-span correlated positively (r _s=0,823, P<0.001) with variation in juvenile survival. The average availability of resources correlated negatively both with the reproductive life-span (r _s=-0.841, P<0.001 after the variation by juvenile survival had been deleted) and variation in juvenile survival (r _s=-0.676, P<0.05).The reproductive effort for female mussels at each site was computed by comparing body weight of reproductive females with body weights of non-reproductive individuals. Availability of resources was much higher in 1976 than in 1975. Consequently, the reproductive effort, an index of the strain of reproduction, was higher in 1975 than in 1976. In 1975 there was a significant correlation between reproductive effort and the length of the reproductive life-span (-0.727, -0.806) and also with the reproductive effort and the variation in juvenile survival (-0.718, -0.758) in females of the length of 60 mm and 70 mm respectively. In 1976, when availability of resources was better, such correlations were not found.Spatial and temporal change in the intake of resources complicates applicability of the principle of resource allocation in the theory of life-history evolution. Studying the mere allocation is not enough if the intake of resources varies in the groups studied. The ratio ovary weight/body weight is a dubious measure of reproductive effort in comparative studies when the input of resources can vary, and this possibility can be ruled out only exceptionally.Correlation between growth and reproductive effort was positive, obviously because both are important components in creating high reproductive capacity. In 1975 reproductive effort increased with size (age). Change in reproductive effort correlated with reproductive life-span (r _s=-0.633, P<0.05).The following parameters occurred together: short reproductive life-span, low age of first reproduction, high reproductive effort, rapid growth and high clutch size. They were realized at sites where the availability of resources was good and variation in juvenile survival was low-i.e. the environment was stable. The results conflict with the prediction of the theory of r and K-selection.     

Selecting for floral character associations in wild radish,Raphanus sativus L.

ESS models of reproductive allocation have been used extensively to explain patterns of floral diversity in angiosperms. These theoretical explorations assume that proportional allocation to pollen, ovules, and seeds, as well as to secondary features such as showy petals and nectar rewards, can evolve independently within the limits set by total resource availability. In populations of California wild radish, we have shown previously that petal size, a strong determinant of visitation by honey bee pollinators, is positively correlated with both pollen and nectar production, but not with ovule or seed number per flower. These phenotypic associations may reflect selection, environmental correlation, and/or genetic constraint. By exerting selection on the petal size : pollen number ratio over two generations, we eliminated the positive correlation between petal size and pollen production, with both characters showing significant change after a single selection episode. Once these two floral traits became uncoupled, nectar sugar production was significantly correlated only with petal size. Our results suggest that natural selection could readily alter reproductive allocation in these flowers, and that the phenotypic correlations observed in nature may be maintained by selection for effective reproductive phenotypes.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Responses to selection on phenoloxidase activity in yellow dung flies

Maintaining an immune system is costly. Resource allocation to immunity should therefore trade off against other fitness components. Numerous studies have found phenotypic trade-offs after immune challenge, but few have investigated genetic correlations between immune components and other traits. Furthermore, empirical evidence for the costs of maintaining an innate immune system in the absence of challenges is rare. We examined responses to artificial selection on phenoloxidase (PO) activity, an important part of the insect innate defense against multicellular pathogens, in yellow dung flies, Scathophaga stercoraria (L.). After 15 generations of successful selection on PO activity, we measured reproductive characters: clutch size, egg hatching rates, adult emergence rates, and adult longevity. We found no evidence for negative genetic correlations between PO activity and reproduction. In fact, flies of lines selected for increased PO activity had larger first clutches, and flies of lines selected for decreased PO activity had smaller ones. However, flies from high-PO lines died earlier than did low-PO flies when no food was available; that is, there is a survival cost of running at high PO levels in the absence of challenge. Variation in resource acquisition or use may lead to positive genetic correlations between PO and fertility and fecundity. The negative correlation between PO and longevity under starvation may indicate that variation for resource acquisition is maintained by a cost of acquisition, based on a genotype-environment interaction.     

Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria

Abstract Considerable effort has been invested in studying the relationship between fitness and genetic variability. While evidence exists both for and against positive genetic variability-fitness correlations (GFC), the possible environment and population-dependency of GFCs has seldom been tested. We investigated GFCs in common frog (Rana temporaria) tadpoles reared under different temperatures and feeding regimes in four replicate populations. Genetic variability in eight microsatellite loci in 238 parents was used to estimate heterozygosity (H) and mean expected d2 in 158-sibships (4515 offspring). Generalized linear mixed model analyses of offspring fitness traits (survival to metamorphosis, developmental and growth rate) revealed that offspring survival probability was positively correlated with H, and that relationships were similar in all four populations tested. However, significant interaction between other genetic variability measures (d2, relatedness) and treatment conditions indicated that GFCs were detectable in some, but not in all environments. Interestingly, GFCs between survival and both heterozygosity and relatedness were most pronounced in stressful environments (i.e. limited food). Developmental and growth rates were significantly associated with d2 but less with H and relatedness. Furthermore, many of these GFCs were population-specific. These results suggest--in line with the contention that expression of inbreeding depression can be environment dependent--that GFCs can also be highly sensitive to the environmental conditions under which they are measured. The results further suggest that the observed positive correlation between H and survival probability is likely to be explainable by the 'general', rather than by the 'local' or 'direct' effect hypotheses.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

Sex allocation under simulated herbivory in the generalist perennial herb Paeonia broteroi (Paeoniaceae)

Theories of optimal resource allocation in flowering plants postulate that allocation to sexual functions are balanced. While many studies have found such evidence in hermaphroditic species among flowers, plants or populations, or at different phenological stages, it has not been supported by other studies. This has been explained by differences among genotypes in ability to acquire resources, resource partitioning among traits unrelated to reproduction or strong selection to maintain positive genetic correlation among traits. I studied how herbivory affected resource allocation to sexual functions in the perennial herb Paeonia broteroi (Paeoniaceae) by measuring a number of floral traits in control plants and in experimental plants under simulated herbivory. The species shows very little plasticity in resource allocation between sexual structures and functions, and appears to be highly sensitive to alterations in the balance of resource acquisition and allocation, with an immediate outcome in terms of seed production and a mid-term response in terms of sprouting and flowering. Plants' ability to collect resources for growth and reproduction before their senescence at the end of the reproductive season, are compromised. This may limit their reproductive potential, the maintenance and growth of their populations, and may influence their demographic state and the plants' ability to respond to selective pressures by external biotic agents.     

Differing amounts of genetic polymorphism in testes and male accessory glands ofDrosophila melanogaster andDrosophila simulans

We surveyed genetic polymorphism by two-dimensional gel electrophoresis of male reproductive tract proteins in 20 isofemale lines each ofDrosophila melanogaster andDrosophila simulans. After classifying 244 such proteins ofDrosophila melanogaster and 271 ofDrosophila simulans by their distribution between testes and accessory glands within the reproductive tract, significant correlations were found between genetic polymorphism and tissue distribution. In both species, gland-specific proteins were significantly more polymorphic than testis-specific proteins, as well as those found in both testes and glands. Simultaneously, inDrosophila simulans, proteins found in roughly equivalent relative abundance in both testes and glands were significantly less variable than gland-specific and testis-specific proteins, as well as those with a quantitative difference in relative abundance between testes and glands. These correlations may reflect general differences in variability between extracellular and intracellular proteins and between proteins with broad as opposed to tissue-specific distributions.We thank the Natural Sciences and Engineering Research Council of Canada for financial support (Grant A0235 to R.S.S.).     

Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus

Environmental manipulations have consistently demonstrated a cost of reproduction in the capital-breeding seed beetle, Callosobruchus maculatus, as females deprived of seeds or mates lay fewer eggs and thereby increase their longevity. Yet fecundity and longevity tend to be positively correlated within populations, perhaps as a consequence of individual differences in resource acquisition. We conducted a split-brood experiment that combined a manipulation of seed availability (seeds present or absent) with a quantitative-genetic analysis of fecundity and lifespan in each environment. Each trait was significantly heritable in each environment. Seed availability not only altered mean fecundity and longevity between environments, but also modified how the traits were correlated within environments. The signs of both the phenotypic and genetic correlations switched from positive when seeds were present to negative when seeds were absent. This reversal persisted even after the effect of body mass (a potential indicator of resource acquisition) was statistically controlled. Cross-environment genetic correlations were positive but significantly less than one for each trait. We suggest that the reversal of the fecundity-longevity relationship depends on a shift in the relative importance of resource-acquisition and resource-allocation loci between environments. In particular, a cost of reproduction may be apparent at the individual level only when seeds are scarce or absent because differences in reproductive effort become large enough to overwhelm differences in resource acquisition. Despite their common dependence on resources acquired during larval stages, fecundity and lifespan in C. maculatus do not appear to be tightly coupled in a physiological or genetic sense.     

Phenotypic plasticity in growth and fecundity induced by strong population fluctuations affects reproductive traits of female fish

Fish are known for their high phenotypic plasticity in life‐history traits in relation to environmental variability, and this is particularly pronounced among salmonids in the Northern Hemisphere. Resource limitation leads to trade‐offs in phenotypic plasticity between life‐history traits related to the reproduction, growth, and survival of individual fish, which have consequences for the age and size distributions of populations, as well as their dynamics and productivity. We studied the effect of plasticity in growth and fecundity of vendace females on their reproductive traits using a series of long‐term incubation experiments. The wild parental fish originated from four separate populations with markedly different densities, and hence naturally induced differences in their growth and fecundity. The energy allocation to somatic tissues and eggs prior to spawning served as a proxy for total resource availability to individual females, and its effects on offspring survival and growth were analyzed. Vendace females allocated a rather constant proportion of available energy to eggs (per body mass) despite different growth patterns depending on the total resources in the different lakes; investment into eggs thus dictated the share remaining for growth. The energy allocation to eggs per mass was higher in young than in old spawners and the egg size and the relative fecundity differed between them: Young females produced more and smaller eggs and larvae than old spawners. In contrast to earlier observations of salmonids, a shortage of maternal food resources did not increase offspring size and survival. Vendace females in sparse populations with ample resources and high growth produced larger eggs and larvae. Vendace accommodate strong population fluctuations by their high plasticity in growth and fecundity, which affect their offspring size and consequently their recruitment and productivity, and account for their persistence and resilience in the face of high fishing mortality.     

Phenotypic plasticity and interpopulation differences in life history traits of<Emphasis Type="Italic"> Armadillidium vulgare</Emphasis> (Isopoda:Oniscidae)

The hypothesis that the balance of trade-offs between survivorship, growth and reproductive allocation in the terrestrial isopod Armadillidium vulgare will change when resource input is increased has been investigated experimentally. When the quality of food available was increased, by adding a mixture of litter from herbaceous dicotyledonous plants to a background low-quality food of dead grasses, survivorship was found to be the most phenotypically plastic trait, increasing by 168%. Growth rates increased by 99% but reproductive allocation by only 21%. In the field, members of a population from a site with more high-quality food grew more than twice as fast as those from a site where less high-quality food was available. The population from the site with higher food availability, contrary to predictions from the laboratory study, did not survive as well as that from the site with less available high-quality food. This may be because the site that is more favourable for growth has a more stressful physical environment due to much bigger temperature fluctuations, which are known to be an important cause of mortality in this species. When individuals from both populations were reared under controlled laboratory conditions, both the parental and F1 generations from the poor growth environment survived better than those from the good growth habitat. However, even when given an excess of high-quality food those from the poor growth environment continued to grow more slowly and had a lower reproductive allocation than those from the site with higher food availability. We conclude that microevolutionary changes may have occurred in the balance of resource allocation between survivorship, growth and reproductive allocation, to favour higher survivorship during the longer prereproductive period at the site where growth to the threshold size for reproduction takes longer.     

Oceanographic drivers of offspring abundance may increase or decrease reproductive variance in a temperate marine fish

In species that reproduce into uncertain environments, the relationship between mean reproductive success (the abundance of new recruits) and the variance in reproductive success (whether adults contribute disproportionally more offspring) may not be straightforward because of stochastic environmental processes that create high variance in reproductive success among adults. In this study, we investigated the relationships between oceanography, reproductive success and reproductive variance in the black rockfish, Sebastes melanops, a long‐lived temperate reef fish with pelagic larvae. We quantified black rockfish recruitment, genetic diversity and growth rates from otolith microstructure over 5 years (2005–2009) during which oceanographic conditions differed. We used cross‐correlations to determine windows of time during which oceanographic variables were significantly correlated with the resulting abundance or genetic diversity of recruits. We found that warmer ocean temperatures were positively correlated with the abundance of recruits, as well as the effective number of breeders. In contrast, the strength of coastal upwelling during settlement was positively correlated with the annual abundance of new recruits, but was negatively correlated with the effective number of breeders. Larval growth rates were explained substantially more by temperature than by upwelling and suggested that temperature affected survival through growth, while upwelling affected survival through transport. Our results indicated that cold ocean temperatures and intense upwelling caused sweepstakes‐like processes to operate on black rockfish populations, despite high abundances of recruits. We propose that a decoupling of the mean and variance in reproductive success may be characteristic of organisms that reproduce into uncertain environments.     

Coevolution between parasite virulence and host life-history traits

Epidemiological models generally explore the evolution of parasite life-history traits, namely, virulence and transmission, against a background of constant host life-history traits. However, life-history models have predicted the evolution of host traits in response to parasitism. The coevolution of host and parasite life-history traits remains largely unexplored. We present an epidemiological model, based on resource allocation theory, that provides an analysis of the coevolution between host reproductive effort and parasite virulence. This model allows for hosts with either a fixed (i.e., genetic) or conditional (i.e., a phenotypically plastic) response to parasitism. It also considers superinfections. We show that parasitism always favors increased allocation to host reproduction, but because of epidemiological feedbacks, the evolutionarily stable host reproductive effort does not always increase with parasite virulence. Superinfection drives the evolution of parasite virulence and acts on the evolution of the host through parasite evolution, generally leading to higher host reproductive effort. Coevolution, as opposed to cases where only one of the antagonists evolves, may generate correlations between host and parasite life-history traits across environmental gradients affecting the fecundity or the survival of the host. Our results provide a theoretical framework against which experimental coevolution outcomes or field observations can be contrasted.     

The evolutionary genetics of acquisition and allocation in the wing dimorphic cricket, Gryllus firmus

The evolutionary trajectories of trade-offs are ultimately governed by the evolution of the underlying physiological processes of the acquisition and subsequent allocation of resources. In this study, we focused directly on acquisition and allocation as traits and estimated their genetic architecture in the trade-off between flight capability and reproduction in the cricket, Gryllus firmus. To determine the evolutionary genetics of acquisition and allocation both within and between resource environments, we performed a large-scale quantitative genetic breeding experiment in which families were split over several resource levels. Our findings were fourfold: (1) there was substantial genetic variance in acquisition and allocation, (2) contrary to the assumption of independence between acquisition and allocation, there was a significant genetic correlation between them, (3) the genetic covariance between acquisition and allocation was significantly different in the different food environments, (4) the trade-off, as measured by the genetic correlation between flight muscle mass and ovary mass, was only significant in the food restriction environments. However, when measured directly as the genetic correlation between reproductive allocation and flight allocation, we found a consistent strong negative genetic correlation, demonstrating that when allocation is measured independently of acquisition we find evidence for the trade-off.     

入侵植物银胶菊在不同生境下表型可塑性和构件生物量

研究了入侵植物银胶菊在4种不同小生境间花果期形态特征变化和构件生物量特征。结果显示:在植株密度小但土壤肥沃的小生境中,植株各形态指标如茎长、茎直径和花序直径等都明显高于其它小生境,在生物量结构特征上则表现为总生物量和花果生物量所占比例的升高。随着植株密度的增加以及土壤肥力下降,上述各形态指标都发生了较明显的变化,生物量投资也进行了优化配置,银胶菊表现出了较高的形态可塑性。银胶菊与觅光和竞争相关的几个指标如叶和根的比例都增加,但用于生殖构件的比例却减少了。相关分析显示,银胶菊花果期各构件生物量与高度成正相关,与密度为负相关,并受环境因素的制约。表明,较高的形态可塑性和较强的生殖配置策略可能是银胶菊成功入侵我国的重要特征。     

The effect of pollination on resource allocation among sexual reproduction,clonal reproduction,and vegetative growth in <Emphasis Type="Italic">Sagittaria potamogetifolia</Emphasis> (Alismataceae)

In order to evaluate the effects of pollination on resource allocation in the marsh herb Sagittaria potamogetifolia, experimental manipulation of pollination efficiency on the pattern of resource allocation was accessed by the proportion of dry weight measurements of sexual, vegetative, and clonal organs. In trials where half of the flowers were pollinated, a significant increase of resource allocated to sexual production and decrease to vegetative production resulted compared to plants that received no pollination. In trials where pollination was 100%, these two reproductive components showed the same trend, but less dramatically. This may support the idea that the trade-offs would be more pronounced when the resource was scarce. Besides, a higher inflorescence production with a lower fruit reproduction occurred as a consequence of decreased pollination level. This increased inflorescence production may be a mechanism to promote outcrossing by enhancing floral attraction or by synchronizing reproductive activity with insect pollinators. Examination for possible trade-offs in resource allocation revealed that there was also a trade-off caused by pollination between fruits plus flowers and bulbils production, which might have detrimental effects on the survival of individuals and populations, but promotes outcrossing and genetic variability.     

Genetic and environmental sources of covariance among internal reproductive traits in the yellow dung fly

Substantial inter- and intraspecific variation is found in reproductive traits, but the evolutionary implications of this variation remain unclear. One hypothesis is that natural selection favours female reproductive morphology that allows females to control mating and fertilization and that diverse male reproductive traits arise as counter adaptations to subvert this control. Such co-evolution predicts the establishment of genetic correlations between male and female reproductive traits that closely interact during mating. Therefore, we measured phenotypic and genetic correlations between male and female reproductive tract characteristics in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), using a nested half-sib breeding experiment. We found significant heritabilities for the size of most reproductive tract traits investigated in both females (spermathecae and their ducts, accessory glands and their ducts) and males (testis size but not sperm length). Within the sexes, phenotypic and genetic correlations were mostly nil or positive, suggesting functional integration of or condition-dependent investment in internal reproductive traits. Negative intrasexual genetic correlations, potentially suggestive of resource allocation trade-offs, were not evident. Intersexual genetic correlations were mostly positive, reflecting expected allometries between male and female morphologies. Most interestingly, testis size correlated positively with female accessory gland size and duct length, potentially indicative of a co-evolutionary arms race. We discuss these and alternative explanations for these patterns of genetic covariance.