Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds?

The variation in breeding-colony size seen in populations of most colonial birds may reflect heritable choices made by individuals who are phenotypically specialized for particular social environments. Although a few studies have reported evidence for genetically based choice of group sizes in birds, we know relatively little about the extent to which animals potentially rely on experience versus innate preferences in deciding with how many conspecifics to settle at different times of their lives. We conducted a cross-fostering experiment in 1997-1998 on cliff swallows (Petrochelidon pyrrhonota) in southwestern Nebraska, USA, in which some individuals were reared in colonies different in size from those in which they were born. Breeding-colony sizes chosen by this cohort of birds were monitored by mark-recapture throughout their lives. A multistate mark-recapture analysis revealed that birds in their first breeding year chose colony sizes similar to those of their birth, regardless of their rearing environment, confirming a previous analysis. Beyond the first breeding year, however, cliff swallows' colony choice was less dependent on where they were born. Birds born in small colonies and reared in large colonies showed evidence of a delayed rearing effect, with these birds overwhelmingly choosing large colonies in later years. Heritabilities suggested strong genetic effects on first-year colony choice but not in later years. Cliff swallows' genetically based colony-size preferences their first year could be a way to ensure matching of their phenotype to an appropriate social environment as yearlings. In later years, familiarity with particular colony sites and available information on site quality may override innate group-size preferences when birds choose colonies.     

Genetic and environmental effects on morphology and fluctuating asymmetry in nestling barn swallows

A barn swallow Hirundo rustica partial cross‐fostering experiment with simultaneous brood size manipulation was conducted in two years with contrasting weather conditions, to estimate heritable variation in tarsus, tail and wing size and fluctuating asymmetry. Environmental stress had contrasting effects depending on trait type. Significant heritabilities for tarsus, tail and wing size were found only in enlarged broods irrespective of year effects, while tarsus asymmetry was significantly heritable in the year with benign weather conditions irrespective of brood size manipulation effects. Tail, wing and composite (multicharacter) asymmetry were never significantly heritable. The environment with the higher heritability generally had higher additive genetic variance and lower environmental variance, irrespective of trait type. Heritability was larger for trait size than for trait asymmetry. Patterns of genetic variation in nestlings do not necessarily translate to the juvenile or adult stage, as indicated by lack of correlation between nestling and fledgling traits.     

Fecundity selection theory: concepts and evidence

Fitness results from an optimal balance between survival, mating success and fecundity. The interactions between these three components of fitness vary depending on the selective context, from positive covariation between them, to antagonistic pleiotropic relationships when fitness increases in one reduce the fitness of others. Therefore, elucidating the routes through which selection shapes life history and phenotypic adaptations via these fitness components is of primary significance to understanding ecological and evolutionary dynamics. However, while the fitness components mediated by natural (survival) and sexual (mating success) selection have been debated extensively from most possible perspectives, fecundity selection remains considerably less studied. Here, we review the theoretical basis, evidence and implications of fecundity selection as a driver of sex‐specific adaptive evolution. Based on accumulating literature on the life‐history, phenotypic and ecological aspects of fecundity, we (i) suggest a re‐arrangement of the concepts of fecundity, whereby we coin the term ‘transient fecundity’ to refer to brood size per reproductive episode, while ‘annual’ and ‘lifetime fecundity’ should not be used interchangeably with ‘transient fecundity’ as they represent different life‐history parameters; (ii) provide a generalized re‐definition of the concept of fecundity selection as a mechanism that encompasses any traits that influence fecundity in any direction (from high to low) and in either sex; (iii) review the (macro)ecological basis of fecundity selection (e.g. ecological pressures that influence predictable spatial variation in fecundity); (iv) suggest that most ecological theories of fecundity selection should be tested in organisms other than birds; (v) argue that the longstanding fecundity selection hypothesis of female‐biased sexual size dimorphism (SSD) has gained inconsistent support, that strong fecundity selection does not necessarily drive female‐biased SSD, and that this form of SSD can be driven by other selective pressures; and (vi) discuss cases in which fecundity selection operates on males. This conceptual analysis of the theory of fecundity selection promises to help illuminate one of the central components of fitness and its contribution to adaptive evolution.     

The trade‐off between fecundity and egg size in a polymorphic population of Arctic charr (Salvelinus alpinus (L.)) in Skogsfjordvatn,subarctic Norway

Reproductive traits differ between intralacustrine Arctic charr morphs. Here, we examine three sympatric lacustrine Arctic charr morphs with respect to fecundity, egg size and spawning time/site to assess reproductive investments and trade‐offs, and possible fitness consequences. The littoral omnivore morph (LO‐morph) utilizes the upper water for feeding and reproduction and spawn early in October. The large profundal piscivore morph (PP‐morph) and the small profundal benthivore morph (PB‐morph) utilize the profundal habitat for feeding and reproduction and spawn in December and November, respectively. Females from all morphs were sampled for fecundity and egg‐size analysis. There were large differences between the morphs. The PB‐morph had the lowest fecundity (mean = 45, SD = 13) and smallest egg size (mean = 3.2 mm, SD = 0.32 mm). In contrast, the PP‐morph had the highest fecundity (mean = 859.5, SD = 462) and the largest egg size (mean = 4.5 mm, SD = 0.46 mm), whereas the LO‐morph had intermediate fecundity (mean = 580, SD = 225) and egg size (mean = 4.3, SD = 0.24 mm). Fecundity increased with increasing body size within each morph. This was not the case for egg size, which was independent of body sizes within morph. Different adaptations to feeding and habitat utilization have apparently led to a difference in the trade‐off between fecundity and egg size among the three different morphs.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.     

Heritable body size mediates apparent life-history trade-offs in a simultaneous hermaphrodite

Physiological trade-offs between life-history traits can constrain natural selection and maintain genetic variation in the face of selection, thereby shaping evolutionary trajectories. This study examines physiological trade-offs in simultaneously hermaphroditic banana slugs, Ariolimax dolichophallus. These slugs have high heritable variation in body size, which strongly predicts the number of clutches laid, hatching success and progeny growth rate. These fitness components were associated, but only when examined in correlation with body size. Body size mediated these apparent trade-offs in a continuum where small animals produced rapidly growing progeny, intermediate-sized animals laid many clutches and large animals had high hatching success. This study uses a novel statistical method in which the components of fitness are analysed in a mancova and related to a common covariate, body size, which has high heritability. The mancova reveals physiological trade-offs among the components of fitness that were previously masked by high variation in body size.     

Selection and constraints on offspring size‐number trade‐offs in sand lizards (Lacerta agilis)

The trade‐off between offspring size and number is a central component of life‐history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade‐off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among‐individual differences can mask individual trade‐offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade‐off between offspring size and number in a population of sand lizards by separating among‐ and within‐individual patterns using a 15‐year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade‐off by investigating how a female's resource (condition)‐ vs. age‐related size (snout‐vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade‐off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade‐off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life‐history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within‐individual patterns can reveal trade‐offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among‐individual variation.     

The evolution of trade-offs: geographic variation in call duration and flight ability in the sand cricket, Gryllus firmus

Quantitative genetic theory assumes that trade-offs are best represented by bivariate normal distributions. This theory predicts that selection will shift the trade-off function itself and not just move the mean trait values along a fixed trade-off line, as is generally assumed in optimality models. As a consequence, quantitative genetic theory predicts that the trade-off function will vary among populations in which at least one of the component traits itself varies. This prediction is tested using the trade-off between call duration and flight capability, as indexed by the mass of the dorsolateral flight muscles, in the macropterous morph of the sand cricket. We use four different populations of crickets that vary in the proportion of macropterous males (Lab = 33%, Florida = 29%, Bermuda = 72%, South Carolina = 80%). We find, as predicted, that there is significant variation in the intercept of the trade-off function but not the slope, supporting the hypothesis that trade-off functions are better represented as bivariate normal distributions rather than single lines. We also test the prediction from a quantitative genetical model of the evolution of wing dimorphism that the mean call duration of macropterous males will increase with the percentage of macropterous males in the population. This prediction is also supported. Finally, we estimate the probability of a macropterous male attracting a female, P, as a function of the relative time spent calling (P = time spent calling by macropterous male/(total time spent calling by both micropterous and macropterous male). We find that in the Lab and Florida populations the probability of a female selecting the macropterous male is equal to P, indicating that preference is due simply to relative call duration. But in the Bermuda and South Carolina populations the probability of a female selecting a macropterous male is less than P, indicating a preference for the micropterous male even after differences in call duration are accounted for.     

Migrate small,sound big: functional constraints on body size promote tracheal elongation in cranes

Organismal traits often represent the outcome of opposing selection pressures. Although social or sexual selection can cause the evolution of traits that constrain function or survival (e.g. ornamental feathers), it is unclear how the strength and direction of selection respond to ecological shifts that increase the severity of the constraint. For example, reduced body size might evolve by natural selection to enhance flight performance in migratory birds, but social or sexual selection favouring large body size may provide a countervailing force. Tracheal elongation is a potential outcome of these opposing pressures because it allows birds to convey an auditory signal of exaggerated body size. We predicted that the evolution of migration in cranes has coincided with a reduction in body size and a concomitant intensification of social or sexual selection for apparent large body size via tracheal elongation. We used a phylogenetic comparative approach to examine the relationships among migration distance, body mass and trachea length in cranes. As predicted, we found that migration distance correlated negatively with body size and positively with proportional trachea length. This result was consistent with our hypothesis that evolutionary reductions in body size led to intensified selection for trachea length. The most likely ultimate causes of intensified positive selection on trachea length are the direct benefits of conveying a large body size in intraspecific contests for mates and territories. We conclude that the strength of social or sexual selection on crane body size is linked to the degree of functional constraint.     

Incubation capacity contributes to constraints on maximal clutch size in Brent Geese Branta bernicla nigricans

Lack ( 1967 ) proposed that clutch size in species with precocial young was determined by nutrients available to females at the time of egg formation; since then others have suggested that regulation of clutch size in these species may be more complex. We tested whether incubation limitation contributes to ultimate constraints on maximal clutch size in Black Brent Geese (Black Brant) Branta bernicla nigricans. Specifically, we investigated the relationship between clutch size and duration of the nesting period (i.e. days between nest initiation and the first pipped egg) and the number of goslings leaving the nest. We used experimental clutch manipulations to assess these questions because they allowed us to create clutches that were larger than the typical maximum of five eggs in this species. We found that the per‐capita probability of egg success (i.e. the probability an egg hatched and the gosling left the nest) declined from 0.81 for two‐egg clutches to 0.50 for seven‐egg clutches. As a result of declining egg success, clutches containing more than five eggs produced, at best, only marginally more offspring. Manipulating clutch size at the beginning of incubation had no effect on the duration of the nesting period, but the nesting period increased with the number of eggs a female laid naturally prior to manipulation, from 25.4 days (95% CI 25.1–25.7) for three‐egg clutches to 27.7 days (95% CI 27.3–28.1) for six‐egg clutches. This delay in hatching may result in reduced gosling growth rates due to declining forage quality during the brood rearing period. Our results suggest that the strong right truncation of Brent clutches, which results in few clutches greater than five, is partially explained by the declining incubation capacity of females as clutch size increases and a delay in hatching with each additional egg laid. As a result, females laying clutches with more than five eggs would typically gain little fitness benefit above that associated with a five‐egg clutch.     

The importance of growth and mortality costs in the evolution of the optimal life history

A central assumption of life history theory is that the evolution of the component traits is determined in part by trade-offs between these traits. Whereas the existence of such trade-offs has been well demonstrated, the relative importance of these remains unclear. In this paper we use optimality theory to test the hypothesis that the trade-off between present and future fecundity induced by the costs of continued growth is a sufficient explanation for the optimal age at first reproduction, alpha, and the optimal allocation to reproduction, G, in 38 populations of perch and Arctic char. This hypothesis is rejected for both traits and we conclude that this trade-off, by itself, is an insufficient explanation for the observed values of alpha and G. Similarly, a fitness function that assumes a mortality cost to reproduction but no growth cost cannot account for the observed values of alpha. In contrast, under the assumption that fitness is maximized, the observed life histories can be accounted for by the joint action of trade-offs between growth and reproductive allocation and between mortality and reproductive allocation (Individual Juvenile Mortality model). Although the ability of the growth/mortality model to fit the data does not prove that this is the mechanism driving the evolution of the optimal age at first reproduction and allocation to reproduction, the fit does demonstrate that the hypothesis is consistent with the data and hence cannot at this time be rejected. We also examine two simpler versions of this model, one in which adult mortality is a constant proportion of juvenile mortality [Proportional Juvenile Mortality (PJM) model] and one in which the proportionality is constant within but not necessarily between species [Specific Juvenile Mortality (SSJM) model]. We find that the PJM model is unacceptable but that the SSJM model produces fits suggesting that, within the two species studied, juvenile mortality is proportional to adult mortality but the value differs between the two species.     

Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major

A brood manipulation experiment on great tits Parus major was performedto study the effects of nestling age and brood size on parentalcare and offspring survival. Daily energy expenditure (DEE)of females feeding nestlings of 6 and 12 days of age was measuredusing the doubly-labeled water technique. Females adjusted theirbrooding behavior to the age of the young. The data are consistentwith the idea that brooding behavior was determined primarilyby the thermoregulatory requirements of the brood. Female DEEdid not differ with nestling age; when differences in body masswere controlled for, it was lower during the brooding periodthan later. In enlarged broods, both parents showed significantlyhigher rates of food provisioning to the brood. Female DEE wasaffected by brood size manipulation, and it did not level offwith brood size. There was no significant effect of nestlingage on the relation between DEE and manipulation. Birds wereable to raise a larger brood than the natural brood size, althoughlarger broods suffered from increased nestling mortality ratesduring the peak demand period of the nestlings. Offspring conditionat fledging was negatively affected by brood size manipulation,but recruitment rate per brood was positively related to broodsize, suggesting that the optimal brood size exceeds the naturalbrood size in this population.     

The interaction of multiple environmental stressors affects adaptation to a novel habitat in the natterjack toad Bufo calamita

The potential to adapt to novel environmental conditions is a key area of interest for evolutionary biology. However, the role of multiple selection pressures on adaptive responses has rarely been investigated in natural populations. In Sweden, the natterjack toad Bufo calamita inhabits two separate distribution areas, one in southernmost Sweden and one on the west coast. We characterized the larval habitat in terms of pond size and salinity in the two areas, and found that the western populations are more affected by both desiccation risk and pond salinity than the southern populations. In a common garden experiment manipulating salinity and temperature, we found that toads from the west coast populations were locally adapted to shorter pond duration as indicated by their higher development and growth rates. However, despite being subjected to higher salinity stress in nature, west coast toads had a poorer performance in saline treatments. We found that survival in the saline treatments in the west coast populations was positively affected by larger body mass and longer larval period. Furthermore, we found negative genetic correlations between body mass and growth rate and their plastic responses to salinity. These results implicate that the occurrence of multiple environmental stressors needs to be accounted for when assessing the adaptive potential of organisms and suggest that genetic correlations may play a role in constraining adaptation of natural populations.     

Body size variation and caste ratios in geographically distinct populations of the invasive big‐headed ant,Pheidole megacephala (Hymenoptera: Formicidae)

Body size is an important life history trait that can evolve rapidly as a result of how species interact with each other and their environment. Invasive species often encounter vastly different ecological conditions throughout their introduced range that can influence relative investment in growth, reproduction and defence among populations. In this study, we quantified variation in worker size, morphology and proportion of majors among five populations of a worldwide invasive species, the big‐headed ant, Pheidole megacephala (Fabricius). The sampled populations differed in ant community composition, allowing us to examine if P. megacephala invests differently in the size and number of majors based on the local ant fauna. We also used genetic data to determine if these populations of P. megacephala represented cryptic species or if morphological differences could be attributed to change following introduction. We found significant variation in worker mass among the populations. Both major and minor workers were largest in Australia, where the ant fauna was most diverse, and minor workers were smallest in Hawaii and Mauritius, where P. megacephala interacted with few to no other ants. We also found differences in major and minor worker morphology among populations. Majors from Mauritius had significantly larger heads (width and length) relative to whole body size than those from Hawaii and Florida. Minors had longer heads and hind tibias in South Africa compared with populations from Australia, Hawaii and Florida. The proportion of majors did not differ among populations, suggesting that these populations may not be subject to trade‐offs in investment in major size versus number. Our molecular data place all samples within the same clade, supporting that these morphologically different populations represent the same species. These results suggest that the variation in shape and morphology of major and minor workers may therefore be the result of rapid adaptation or plastic responses to local conditions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 423–438.     

Short‐ and long‐term costs of reproduction in a migratory songbird

Costs of reproduction represent a common life‐history trade‐off. Critical to understanding these costs in migratory species is the ability to track individuals across successive stages of the annual cycle. We assessed the effects of total number of offspring fledged and date of breeding completion on pre‐migratory body condition, the schedule of moult and annual survival in a migratory songbird, the Savannah Sparrow Passerculus sandwichensis. Between 2008 and 2010, moult was delayed for individuals that finished breeding later in the breeding period and resulted in reduced lean tissue mass during the pre‐migratory period, suggesting an indirect trade‐off between the timing of breeding completion and condition just prior to migration. Lean tissue mass decreased as the number of offspring fledged increased in 2009, a particularly cool and wet year, illustrating a direct trade‐off between reproductive effort and condition just prior to migration in years when weather is poor. However, using a 17‐year dataset from the same population, we found that parents that fledged young late in the breeding period had the highest survival and that number of offspring fledged did not affect survival, suggesting that individuals do not experience long‐term trade‐offs between reproduction and survival. Taken together, our results suggest that adult Savannah Sparrows pay short‐term costs of reproduction, but that longer‐term costs are mitigated by individual quality, perhaps through individual variation in resource acquisition.     

Rainbow trout in seasonal environments: phenotypic trade‐offs across a gradient in winter duration

Survival through periods of resource scarcity depends on the balance between metabolic demands and energy storage. The opposing effects of predation and starvation mortality are predicted to result in trade‐offs between traits that optimize fitness during periods of resource plenty (e.g., during the growing season) and those that optimize fitness during periods of resource scarcity (e.g., during the winter). We conducted a common environment experiment with two genetically distinct strains of rainbow trout to investigate trade‐offs due to (1) the balance of growth and predation risk related to foraging rate during the growing season and (2) the allocation of energy to body size prior to the winter. Fry (age 0) from both strains were stocked into replicate natural lakes at low and high elevation that differed in winter duration (i.e., ice cover) by 59 days. Overwinter survival was lowest in the high‐elevation lakes for both strains. Activity rate and growth rate were highest at high elevation, but growing season survival did not differ between strains or between environments. Hence, we did not observe a trade‐off between growth and predation risk related to foraging rate. Growth rate also differed significantly between the strains across both environments, which suggests that growth rate is involved in local adaptation. There was not, however, a difference between strains or between environments in energy storage. Hence, we did not observe a trade‐off between growth and storage. Our findings suggest that intrinsic metabolic rate, which affects a trade‐off between growth rate and overwinter survival, may influence local adaptation in organisms that experience particularly harsh winter conditions (e.g., extended periods trapped beneath the ice in high‐elevation lakes) in some parts of their range.     

Development and the effects of extended parenting in the cold‐breeding burying beetle Nicrophorus sayi

1. Burying beetles (Nicrophorus spp.) provide an excellent model system to test predictions about the relationships between environment, life‐history and behaviour. All species in the genus display similar natural histories, breeding on vertebrate carcasses and providing parental care to developing offspring. However, variations in other aspects of species' ecologies provide a rich framework to examine the evolution of parental behaviours and other traits. 2. One little‐studied species, N. sayi, breeds in substantially colder temperatures than its congeners, creating a potentially harsh environment for offspring. Here, we examined the timing of reproductive and developmental events in this species, and also investigated the effects of removing parents on offspring performance. 3. We find that development is not only extremely slow in this species, but it is also delayed even in comparison to other burying beetles reared at similar temperatures. However, the presence of parents reduces the time that offspring take to leave the carcass. This decrease in development time does not appear to result in a trade‐off with mortality or body size. 4. From these results, we suggest that very slow development may be advantageous when living in a particularly cold environment. Additionally, one role of extended parental care may be to assist offspring in dealing with these harsh conditions, and to mitigate the potentially negative consequences of adopting such a slow life‐history strategy.     

Life‐history strategy varies with the strength of competition in a food‐limited ungulate population

Fluctuating population density in stochastic environments can contribute to maintain life‐history variation within populations via density‐dependent selection. We used individual‐based data from a population of Soay sheep to examine variation in life‐history strategies at high and low population density. We incorporated life‐history trade‐offs among survival, reproduction and body mass growth into structured population models and found support for the prediction that different life‐history strategies are optimal at low and high population densities. Shorter generation times and lower asymptotic body mass were selected for in high‐density environments even though heavier individuals had higher probabilities to survive and reproduce. In contrast, greater asymptotic body mass and longer generation times were optimal at low population density. If populations fluctuate between high density when resources are scarce, and low densities when they are abundant, the variation in density will generate fluctuating selection for different life‐history strategies, that could act to maintain life‐history variation.