The maintenance of phenotypic and genetic variation in threshold traits by frequency-dependent selection

Many traits are phenotypically dimorphic but determined by the action of many loci, the phenotype being a result of a threshold of sensitivity. Quantitative genetic analysis has shown that generally there is considerable additive genetic variation for the trait, the average heritability being 0.52. In numerous cases threshold traits have been shown, or are assumed, to be under frequency-dependent selection; examples include satellite-territorial behaviour, sex-determination, wing dimorphism and trophic dimorphism. In this paper I investigate the potential for frequency-dependent selection to maintain both phenotypic and additive genetic variation in threshold traits. The qualitative results are robust to the particular form of the frequency-dependent selection function. The equilibrium proportion is more or less independent of population size but the heritability increases with population size, typically approaching its maximal value at a population size of 5000, when the mutation rate is 10^?4. A tenfold decrease in the mutation rate requires an approximate doubling of the population size before an asymptotic value is approached. Thus frequency-dependent selection can account for both the existence of two morphs in a population and the observed levels of heritability. It is also shown, both via simulation and theory, that the quantitative genetic model and a simple phenotypic analysis predict the same equilibrium morph proportion.     

Multi-trophic effects of ungulate intraguild predation on acorn weevils

Predators and parasitoids may contribute to controlling the population sizes of phytophagous insects, and this has been shown to benefit plants. Phytophagous insects may also be killed by other herbivores (intraguild predation), usually larger-sized vertebrates that ingest insects accidentally while feeding on common food sources. We studied the intraguild predation on acorn weevils by ungulates and assessed the consequences for weevil populations. Infested acorns are prematurely abscised and the weevil larvae finish their development inside the acorns after being dropped. Our results show that weevil larvae were killed by ungulates eating the infested acorns on the ground. Ungulates did not discriminate between infested and sound acorns, and the probability of a larva being incidentally eaten was inversely related to acorn availability. Thus, predation risk was enhanced by the premature drop of infested acorns when acorn availability on the ground was low. Predation rates on infested acorns were much higher where ungulates were present, and acorn infestation rates were significantly lower. However, ungulates did not provide the oaks any net benefit, since the reduction of infestation rates was not enough to compensate for the large amounts of sound acorns eaten by ungulates. Seed predation is usually studied as a progressive loss of seeds by pre- and post-dispersal predators, but the interactions between them are usually not considered. We show that intraguild predation on insects by large ungulates had an effect on the structure of the foraging guild, as the proportion of acorns predated by insects decreased; however, replicating the same experimental design in different ecological scenarios would increase the strength of these results. In conclusion, the present study shows the importance of considering the multi-trophic interactions between seed predators in order to have a complete picture of granivory.     

Within-stream variation in early life-history traits in brown trout

Significant additive genetic variance for most early life-history traits was found in brown trout Salmo trutta living in both allopatry above an impassable waterfall and sympatry (below the waterfall in the same stream) with alpine bullhead Cottus poecilopus. These traits included length, mass and yolk sac volume at hatching, and size at'button-up' (the time when yolk is enclosed within the body cavity). There were small differences in size at hatching and size at button-up among populations (adjusted for egg size). However, sympatric fry grew more rapidly and experienced lower mortality rates during the period of first feeding than allopatric fry. This might indicate behavioural differences between brown trout from the two populations. It is suggested that these phenotypic differences may be a result of adaptation to living in sympatry with alpine bullhead.     

Host selection and responses to forest fragmentation in acorn weevils: inferences from dynamic occupancy models

Prior studies on species‐specific responses to habitat alteration have demonstrated that niche breadth is positively associated with patch occupancy rates in landscapes fragmented by agriculture. However, these studies generally have focused on vertebrates and relied upon data collected at a single point in time, neglecting dynamic processes that could alter inferences. We studied the effects of host selection and forest fragmentation on population dynamics of acorn weevils Curculio, the primary insect seed predators of oaks in North America. Detection/non‐detection data were collected from 174 red and white oaks in 19 forested fragments from 2005–2008. We used dynamic multi‐season site‐occupancy models within a Bayesian framework to explore variation in patch (tree‐level) occupancy dynamics of three species of weevils that vary in their specialization, i.e. their relative selection of red and white oak as hosts: C. pardalis (white oak specialist), C. sulcatulus (generalist) and C. proboscideus (generalist). Contrary to expectations, the specialist exhibited greater estimated rates of occupancy than generalists. However, red oak trees occupied by the white oak specialist appeared to function as sink populations maintained by frequent colonization following local extinction. Specialists also exhibited greater relative variation in occupancy and relative abundance on their host trees among years. Generalists exhibited lower local extinction and colonization rates than the specialist. Occupancy and vital rates of weevils on a host tree increased with acorn production and were significantly influenced by neighborhood forest density. Our results suggest that across much of their range in the eastern United States acorn weevils exist in fragmented, temporally dynamic landscapes, with generalists occurring on a lower proportion of usable trees but buffered by access to more suitable patches and greater patch‐specific survival. More generally, our results demonstrate that estimates of specialization derived from occupancy data may be misleading in the absence of patch‐specific information on vital rates.     

Large-scale intraspecific variation in life-history traits of European freshwater fish

Aims To test the magnitude and direction of the effects of large‐scale environmental factors (latitude and habitat type: lotic or lentic) on the intraspecific variations in multiple life‐history traits, across multiple European freshwater fish species. To test the relevance of defining species traits by quantifying the magnitude of interspecific vs. intraspecific variability in traits. Location Europe. Methods We obtained estimates of 11 fish traits from published sources for 1089 populations of 25 European freshwater fish species. Traits were: longevity, maximal length, growth rate, asymptotic length, mortality rate, age and length at maturation, fecundity, egg size, gonadosomatic index, and length of breeding season. We described population habitats by latitude and habitat type (lotic or lentic), when available. For each species we tested the combined effect of latitude and habitat type on the intraspecific variation of each trait using analysis of covariance (ancova ). We compared the intraspecific variation in traits with the variation between species using an analysis of variance (anova ) for each trait, all species pooled. Results We found a consistent effect in direction of latitude on six traits, but we showed that this effect is not always significant across species. Higher‐latitude populations often grew more slowly, matured later, had a longer life span and a higher maximal and asymptotic length, and allocated more energy to reproduction than populations at lower latitudes. By contrast, we noted only a slight effect of habitat type on the intraspecific variation in traits, except for Salmo trutta. All traits varied significantly between species. However, traits such as growth rate, mortality rate and length of breeding season varied more between populations than between species, whereas fecundity and traits associated with body length varied more between species. Main conclusions Latitude, in contrast to habitat type, is an important factor influencing several traits of geographically widely dispersed populations of multiple European freshwater fish species. Species traits that vary more between species than between populations are attractive variables for understanding and predicting the responses of stream fish communities to their environment.     

The components of life-history traits variation in Daphnia magna population

The variation of six growth and reproduction traits in the parthenogenetic clones of Daphnia magna and its relationships with the genotypes at 5 isozyme loci were studied under controlled conditions at three food concentrations. A significant genetic component of age at maturity, growth rate and fecundity variation was detected. Nested ANOVA revealed the influences of the genotypes of the isozyme loci, that are more pronounced at the high food concentration. In some cases the genotype-environment interactions were found.The variation of body length at 6 days and total number of offspring includes a significant heterozygosity — environment interaction. The most heterozygous clones show the least differences in life history traits between food conditions.Life-history traits heritability, genotype-environment interactions and different reproductive strategies of the clones are discussed.     

Lifetime selection on heritable life-history traits in a natural population of red squirrels

Abstract Despite their importance in evolutionary biology, heritability and the strength of natural selection have rarely been estimated in wild populations of iteroparous species or have usually been limited to one particular event during an organism's lifetime. Using an animal-model restricted maximum likelihood and phenotypic selection models, we estimated quantitative genetic parameters and the strength of lifetime selection on parturition date and litter size at birth in a natural population of North American red squirrels, Tamiasciurus hudsonicus. Litter size at birth and parturition date had low heritabilities ( h² = 0.15 and 0.16, respectively). We considered potential effects of temporal environmental covariances between phenotypes and fitness and of spatial environmental heterogeneity in estimates of selection. Selection favored early breeders and females that produced litter sizes close to the population average. Stabilizing selection on litter size at birth may occur because of a trade-off between number of offspring produced per litter and offspring survival or a trade-off between a female's fecundity and her future reproductive success and survival.     

Realized correlated responses to artificial selection on pre-adult life-history traits in a butterfly

We use artificial selection experiments targeted on egg size, development time or pupal mass within a single butterfly population followed by a common-garden experiment to explore the interactions among these life-history traits. Relationships were predicted to be negative between egg size and development time, but to be positive between development time and body size and between egg size and body size. Correlated responses to selection were in part inconsistent with these predictions. Although there was evidence for a positive genetic correlation between egg and body size, there was no support for genetic correlations between larval development time and either egg size or pupal mass. Phenotypic correlations among the three target traits of selection gave comparable results for the relationships between egg mass and development time (no association) as well as between egg mass and pupal mass (positive association), but not for the relation between development time and pupal mass (negative phenotypic correlation). In summary, correlated responses to selection as well as phenotypic correlations were rather unpredictable. The impact of variation in acquisition and allocation of energy as well as of the benign conditions used deserve further investigation.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

Geographic variation in the effects of temperature on life-history traits in the large milkweed bug Oncopeltus fasciatus

Summary Complete sets of life-history data (sufficient to construct life-tables and calculate intrinsic rates of increase) were collected at each of three constant temperatures for descendants of two tropical populations of the Large Milkweed Bug, Oncopeltus fasciatus. Although the two populations occur only about 60 km apart, they experience quite different thermal regimes, with little variation in mean monthly temperature at either site. In addition to the pronounced effect of ambient temperature on life-history traits, significant population-by-temperature interactions were observed for six of the eight traits examined. The data and the recent history of the species' distribution are consistent with the hypothesis that natural selection in the cool habitat has favored improved survival and increased reproduction at cool temperatures, with some trade-offs with respect to performance at higher (but ecologically relevant) temperatures.     

New perspectives on the evolution of exaggerated traits

The scaling of body parts is central to the evolution of morphology and shape. Most traits scale proportionally with each other and body size such that larger adults are essentially magnified versions of smaller ones. This pattern is so ubiquitous that departures from it – disproportionate scaling between trait and body size – pique interest because it can generate dramatically exaggerated traits. These extreme morphologies are frequently hypothesized to result from sexual selection and their study has a long history, with several hypotheses seeking to explain their evolution. Despite this effort, surprisingly little progress has been made in demonstrating the forms of selection that produce different scaling patterns or in identifying the mechanisms that underlie the expression and evolution of scaling relationships. Here we review recent insights regarding the proximate mechanisms that regulate and integrate trait growth and that offer a new framework for studying the evolution of morphological scaling.     

Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits

The relative importance of genetic, environmental, and maternal effects as determinants of geographical variation in vertebrate life-histories has not often been explored. We examined the role of genetic and maternal effects as determinants of population divergence in survival and three important larval life-history traits (growth rate, age, and size at metamorphosis) using reciprocal crosses between two latitudinally separated populations of the common frog ( Rana temporaria Linnaeus). Genetic effects were important in all three traits as indicated by the significant effect of male origin, but there was also evidence for nonadditive genetic contributions on metamorphic size and growth rate. Likewise, maternal effect contributions to population divergence were large, partially environment dependent, and apparently acting primarily through egg size in two of three traits. These results suggest that both genetic and maternal effects are important determinants of geographical variation in amphibian life-histories, and that much of the differentiation resulting from maternal effects is mediated through variation in egg size. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 61–70.     

Natural selection on female life-history traits in relation to socio-economic class in pre-industrial human populations

Life-history theory predicts that resource scarcity constrains individual optimal reproductive strategies and shapes the evolution of life-history traits. In species where the inherited structure of social class may lead to consistent resource differences among family lines, between-class variation in resource availability should select for divergence in optimal reproductive strategies. Evaluating this prediction requires information on the phenotypic selection and quantitative genetics of life-history trait variation in relation to individual lifetime access to resources. Here, we show using path analysis how resource availability, measured as the wealth class of the family, affected the opportunity and intensity of phenotypic selection on the key life-history traits of women living in pre-industrial Finland during the 1800s and 1900s. We found the highest opportunity for total selection and the strongest selection on earlier age at first reproduction in women of the poorest wealth class, whereas selection favoured older age at reproductive cessation in mothers of the wealthier classes. We also found clear differences in female life-history traits across wealth classes: the poorest women had the lowest age-specific survival throughout their lives, they started reproduction later, delivered fewer offspring during their lifetime, ceased reproduction younger, had poorer offspring survival to adulthood and, hence, had lower fitness compared to the wealthier women. Our results show that the amount of wealth affected the selection pressure on female life-history in a pre-industrial human population.     

Regional variation in seasonality affects migratory behaviour and life-history traits of two Mediterranean passerines

Migratory birds may improve fecundity by moving to seasonal breeding areas, but may also suffer higher mortality rates as a cost of movement. However, the covariation among seasonality, migratoriness and life histories should change between species if their ecological features affect site-tenacity, survival or fecundity. In frugivorous birds, for instance, wandering in search of fruits may trigger broader migrations than territorial defence, and also may improve nonbreeding survival by preventing food shortages that eventually happen in discrete territories. We studied the variation in spatio-temporal distribution, life expectancy and fecundity in robins (Erithacus rubecula) and blackcaps (Sylvia atricapilla) distributed in three Iberian regions with a low, mid or high degree of environmental seasonality. In the Iberian Peninsula, robins and blackcaps are the two most intensive frugivores in winter; however, robins are territorial while blackcaps track fruit abundance among habitat patches. In the most seasonal area, robins and blackcaps decreased abundance in winter and showed a lower breeding-site tenacity, a shorter life expectancy and a larger clutch size. However, blackcaps tended to be more migratory than robins in all regions. Despite their stronger migratory behaviour, blackcaps showed a longer life expectancy and a smaller clutch size than robins in all regions. In robins, winter territoriality could decrease nonbreeding survival but also improve fecundity, because survivors are dominant and hence more efficient breeders. In blackcaps, however, the use of the most profitable habitat patches could improve nonbreeding survival, thereby allowing a similar recruitment than in robins with a lower reproductive investment. These results support that regional-scale changes in seasonality may affect migratory behaviour and hence the tradeoff between reproduction and survival in birds, doing so differently depending on the idiosyncrasy of each species.     

Chemical defence in a sawfly: genetic components of variation in relevant life-history traits

Larvae of several tenthredinid sawfly species readily release droplets of haemolymph through their integument when attacked by predators. This defence mechanism via 'bleeding' is characterised by a low integument resistance and a high haemolymph deterrence. Both traits are variable, and negatively correlated among species. We sought to determine if such differences in the propensity to bleed also occur intraspecifically by studying the heritability of traits potentially associated with the bleeding phenomenon in the turnip sawfly Athalia rosae ruficornis Jakovlev (Hymenoptera: Tenthredinidae, Allantinae). For three European populations, heritabilities were estimated in the laboratory in a parent-offspring and a full-sib design for haemolymph deterrence (measured as concentration of sequestered glucosinolate), integument resistance, body mass of eonymph and adult, and developmental time. Within A. rosae, no significant negative phenotypic correlation was found between the two traits directly related to the defence mechanism: integument resistance and haemolymph deterrence. However, the significant heritabilities found for these traits in the full-sib analysis (0.39 and 0.35, respectively, for males in the Swiss population) show that the variation has a genetic component. While full-sib analysis revealed highly significant heritabilities for most traits in all the three populations, parent-offspring regression revealed little or no evidence of heritable variation. Effects of common environment for siblings and variation in the host-plant quality between insect generations are likely to be the main factors explaining these differences. A consequence of such host-plant variation in the wild might be that genetic variation of such chemical defensive traits is largely invisible to natural selection.     

Small-scaled geographical variation in life-history traits of the blowfly Calliphora vicina between rural and urban populations

The impact of the urban heat-island effect, the warming-up of an urban area caused by human activity, on the blowfly Calliphora vicina Robineau-Desvoidy (Diptera: Calliphoridae) was examined at two British sites, 30 km apart. Waterloo in Central London is a highly urbanised built-up area, whereas Box Hill in the county of Surrey is a rural pasture and woodland location. The phenotypic plasticity of 12 C. vicina cultures, originated from single females from each of the two sites, was measured using three developmental characters: adult body size (represented as the length of the cross vein dm-cu of the right wing), development time as accumulated degree-days (ADD), and growth rate (length of dm-cu/ADD), along a constant temperature series of 16, 20, 24, and 28 °C in the laboratory. The blowflies from Box Hill had the same ADD as those from Waterloo, but showed a significantly larger adult size and growth rate at lower temperatures, suggesting the existence of local adaptations that may be caused by the differing levels of urbanisation between the two studied sites. Not surprisingly, a trade-off between adult size and development time was found. Females showed longer development times than males at all four temperatures, indicating they may need to ingest more food as larvae to furnish ovarioles and increase fecundity. However, females had larger adult size than males at 16 and 20 °C but a reverse at 28 °C, suggesting that females may be more cold-adapted than males.     

Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits

Predicting the spread of invasive species is a challenge for modern ecology. Although many invasive species undergo genetic bottlenecks during introduction to new areas resulting in a loss of genetic diversity, successful invaders manage to flourish in novel environments either because of pre-adaptations or because important traits contain adaptive variation enabling rapid adaptation to changing conditions. To predict and understand invasion success, it is crucial to analyse these features. We assessed the potential of a well-known invader, the Colorado potato beetle (Leptinotarsa decemlineata), to expand north of its current range in Europe. A short growing season and harsh overwintering conditions are apparent limiting factors for this species’ range. By rearing full-sib families from four geographically distinct populations (Russia, Estonia, Poland, Italy) at two fluctuating temperature regimes, we investigated (a) possible differences in survival, development time, and body size among populations and (b) the amount of adaptive variation within populations in these traits. All populations were able to complete their development in cooler conditions than in their current range. A significant genotype–environment interaction for development time and body size suggests the presence of adaptive genetic variation, indicating potential to adapt to cooler conditions. The northernmost population had the highest survival rates and fastest development times on both temperature regimes, suggesting pre-adaptation to cooler temperatures. Other populations had minor differences in development times. Interestingly, this species lacks the classical trade-off between body size and development time which could have contributed to its invasion potential. This study demonstrates the importance of considering both ecological and evolutionary aspects when assessing invasion risk.     

Latitudinal variation of life-history traits of an exotic and a native impatiens species in Europe

Understanding the responses of invasive and native populations to environmental change is crucial for reliable predictions of invasions in the face of global change. While comparisons of responses across invasive species with different life histories have been performed before, comparing functional traits of congeneric native and invasive species may help to reveal driving factors associated with invasion. Here we compared morphological functional trait patterns of an invasive species (Impatiens parviflora) with its congeneric native species (I. noli-tangere) along an approximately 1600 km European latitudinal gradient from France (49°34′N) to Norway (63°40′N). Soil nitrogen was recorded during six weeks of the growing season, and light, soil moisture, and nutrient availability were estimated for each sampled population using community weighted means of indicator values for co-occurring species. Temperature data were gathered from nearby weather stations.Both the native and invasive species are taller at higher latitudes and this response is strongest in the invasive species. Seed mass and number of seeds per capsule increase in I. noli-tangere but decrease in I. parviflora towards higher latitudes. Surprisingly, plant height in the invasive I. parviflora decreases with increasing soil nitrogen availability. The latitudinal pattern in seed mass is positively related to temperature in I. noli-tangere and negatively in I. parviflora. Leaf area of both species decreases with increasing Ellenberg indicator values for nitrogen and light but increases with increasing soil moisture. Soil nitrogen concentrations and Ellenberg indicator values for nitrogen have significant positive (I. noli-tangere) and negative (I. parviflora) effects on the number of seeds per capsule. Our results show that the native I. noli-tangere has efficient reproduction at its range edge while the invasive I. parviflora shows a marked decrease in seed size and seed number per capsule. These patterns are unrelated to the growth and obtained size of the plants: even low soil nitrogen availability in the north seemed not to limit plant growth and size. Our results suggest that the invasive I. parviflora tends to become more invasive at lower latitudes by producing heavier seeds and more seeds per capsule.     

Spatial and temporal variation in a suite of life-history traits in two species of wolf spider

Abstract.  1. Life-history traits and density were assayed in seven populations of two sympatric species of wolf spider for three consecutive years. The goal of the study was to quantify population dynamics and its relation to spatial and temporal life-history variation.
2. Adult female body size and fecundity varied significantly, among field sites and among years, in both species. Female spiders of both species differed in mean relative reproductive effort among sites, but not among years. The size of offspring was invariable, with no significant differences due to site or year.
3. All populations of both species tended to either decrease or increase in density during a given year and this was tightly correlated with changes in prey consumption rates.
4. Since life-history patterns are determined primarily by selection, it is concluded that size at sexual maturity for females is phenotypically plastic and responds to changes in prey availability. Offspring size however is not plastic and it is likely that other selection forces have determined offspring size. Temporal fluctuations in population size are correlated over a large area relative to dispersal capabilities for these species and conservation efforts for invertebrates must take this into consideration.     

Natural selection and quantitative genetics of life-history traits in Western women: a twin study

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection will cause a change among women in a contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the "baby boom" phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.