Evaluation of offspring size–number invariants in 12 species of lizard

The optimal division of resources into offspring size vs. number is one of the classic problems in life‐history evolution. Importantly, models that take into account the discrete nature of resource division at low clutch sizes suggest that the variance in offspring size should decline with increasing clutch size according to an invariant relationship. We tested this prediction in 12 species of lizard with small clutch sizes. Contrary to expectations, not all species showed a negative relationship between variance in offspring size and clutch size, and the pattern significantly deviated from quantitative predictions in five of the 12 species. We suggest that the main limitation of current size–number models for small clutch sizes is that they rely on assumptions of hierarchical allocation strategies with independence between allocation decisions. Indeed, selection may favour alternative mechanisms of reproductive allocation that avoid suboptimal allocation imposed by the indivisible fraction at low clutch sizes.     

Evolutionary response to selection on clutch size in a long-term study of the mute swan

Life-history traits in wild populations are often regarded as being subject to directional selection, and the existence of substantial variation and microevolutionary stasis of these characters is therefore a problem in need of explanation. Avian clutch size is an archetypal life-history trait in this context, and many studies have sought to test explanations for stasis in clutch size. Surprisingly, there are many fewer studies that used long-term data to ask how selection acts on clutch size, particularly in a multivariate framework. In this article, we report selection, inheritance, and evolution of clutch size over 25 years in a colony of mute swans using a multivariate quantitative genetic framework to control for correlations with breeding time. We show that clutch size is influenced by both additive genetic and permanent environmental effects and that selection acts on clutch size in combination with breeding time. Natural selection on clutch size is strongly directional, favoring larger clutches, and we observe an increase in clutch size of 0.35 standard deviations, consistent with the expected response based on selection and inheritance of clutch size. We hypothesize that these changes result from recent relaxation of food constraints and predation risks experienced by this colony.     

Natural selection and inheritance of breeding time and clutch size in the collared flycatcher

Many characteristics of organisms in free-living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often-cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long-term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation ("animal models") to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent-offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2 = 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA = -0.41 +/- 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (beta = -0.28 +/- 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (beta = -0.20 +/- 0.04), but not on clutch size (beta = 0.03 +/- 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life-history trade-offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life-history trade-offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.     

COSTS OF REPRODUCTION IN THE WILD: PATH ANALYSIS OF NATURAL SELECTION AND EXPERIMENTAL TESTS OF CAUSATION

During 1991 through 1994, natural selection on reproductive effort in side-blotched lizards was indexed by measuring total clutch mass produced on the first clutch of the reproductive season and assessing how such effort in current reproduction affects subsequent survival and clutch production. In addition, selection was also experimentally assessed in free-ranging female side-blotched lizards by (1) surgically decreasing total clutch mass (direct ovarian manipulation) and enhancing clutch mass using (2) exogenous gonadotropin, and (3) exogenous corticosterone. Surgical reduction of clutch mass uniformly enhanced survival. However, increasing clutch mass had more complex effects depending on year. Experimentally enhanced clutch mass enhanced survival in 1991, had no effect on survival in 1992, and decreased survival in 1993. Despite the complexity of these experimental results, they are corroborated by our comparative data. It is important to note that local environmental effects can obscure detection of costs arising from natural variation in reproductive effort, and we removed such effects using path analysis. The striking shift in natural selection favoring females laying a large clutch mass (1991) to selection against females laying a large clutch mass (1993) is associated with an end of a severe multiyear drought. Our natural-history observations suggest that the correlated increase in predatory snake activity on our study site, coincident with the end of the drought, is the agent of natural selection. Although the actual agents of selection (e.g., snake predation versus drought-related effects) are not resolved, the patterns of natural selection measured in our comparative and experimental data are also consistent with year-to-year changes in clutch mass and egg size that would be indicative of rapid short-term evolution in these traits.     

Nonsiblicidal behavior and the evolution of clutch size in bethylid wasps

Parent-offspring conflict over clutch size may lead to siblicidal behavior between juveniles. In parasitoid wasps, selection for siblicide in small broods is predicted to produce a dearth of gregarious broods with few eggs. Here we document the clutch size distribution in the Bethylidae, a large family of aculeate parasitoids. Small gregarious clutches are the most common. Further data suggest that the most common gregarious clutches in the parasitoid Hymenoptera as a whole contain only a few eggs. Across bethylid species, both clutch size and wasp size increase with host size. Within genera clutch size is more closely related to host size, but between genera or larger clades wasp size is more closely related to host size. The volume of the emerging wasp brood does not depend on whether a species lays single- or multiple-egg clutches once host size is taken into account. These data suggest that clutch size in bethylid wasps is best described by traditional optimality models and that siblicide plays little role in this and possibly other families. We propose several ecological reasons for the rarity of siblicide in bethylids: ectoparasitism, idiobiosis, and a suite of characteristics associated with high within-brood relatedness.     

Multitasking and the evolution of optimal clutch size in fluctuating environments

Adaptive studies of avian clutch size variation across environmental gradients have resulted in what has become known as the fecundity gradient paradox, the observation that clutch size typically decreases with increasing breeding season length along latitudinal gradients, but increases with increasing breeding season length along elevational gradients. These puzzling findings challenge the common belief that organisms should reduce their clutch size in favor of additional nesting attempts as the length of the breeding season increases, an approach typically described as a bet‐hedging strategy. Here, we propose an alternative hypothesis—the multitasking hypothesis—and show that laying smaller clutches represents a multitasking strategy of switching between breeding and recovery from breeding. Both our individual‐based and analytical models demonstrate that a small clutch size strategy is favored during shorter breeding seasons because less time and energy are wasted under the severe time constraints associated with breeding multiply within a season. Our model also shows that a within‐generation bet‐hedging strategy is not favored by natural selection, even under a high risk of predation and in long breeding seasons. Thus, saving time—wasting less time as a result of an inability to complete a breeding cycle at the end of breeding season—is likely to be the primary benefit favoring the evolution of small avian clutch sizes during short breeding seasons. We also synthesize the seasonality hypothesis (pronounced seasonality leads to larger clutch size) and clutch size‐dependent predation hypothesis (larger clutch size causes higher predation risks) within our multitasking hypothesis to develop an integrative model to help resolve the paradox of contrasting patterns of clutch size along elevational and latitudinal gradients. Ultimately, our models provide a new perspective for understanding life‐history evolution under fluctuating environments.     

Predation risk induces changes in nest-site selection and clutch size in the Siberian jay

Life-history theory predicts that an individual should reduce its reproductive efforts by laying a smaller clutch size when high risk of nest predation reduces the value of current reproduction. Evidence in favour of this 'nest predation hypothesis', however, is scarce and based largely on correlative analyses. Here, we manipulated perceived risk of nest predation in the Siberian jay Perisoreus infaustus using playback involving a mixture of calls by corvid nest predators in the vicinity of nest sites. In response to being exposed to this acoustic cue simulating increased risk of nest predation, the jays chose a nest site offering more protective covering and reduced clutch size. This is the first experimental demonstration of clutch size adjustment and nest site selection as a result of phenotypic plasticity in an open nesting passerine reflecting a facultative response to the perceived risk of nest predation.     

Ecological correlates and heritability of reproductive variation in two co-occurring grasshopper species

ABSTRACT. 1. Relationships are examined between mean egg size and possible selection pressures acting on two grasshopper species, Chorthippus brunneus (Thunb.) and Myrmeleotettix maculatus (Thunb.), co-occurring at three sites in a sand dunes area.
2. Heavy eggs were laid where the mean crowding of hatchlings was high in relation to the amount of grasses with thin-edged leaves. To a lesser extent, large eggs were also found in more desiccating conditions. Mean egg dry weights did not correlate with measures of crowding or measures of crowding in relation to total grass abundance.
3. Significant differences in egg size and clutch sizes were observed between the stocks of second generation, laboratory-reared M.maculatus from three study sites. The significant difference in egg size (site 2 stock > site 1 stock) ran counter to the difference observed in the field but the difference in clutch size (site 3< site 2) was consistent with that observed between field populations.
4. We argue that egg size is primarily determined by selection pressures on the size of hatchlings but that predictably poor feeding conditions for juveniles and adults at site 2 results in the production of smaller adults which, in M.maculatus , then lay smaller eggs. We further argue that M. maculatus from site 2 have been selected to lay larger eggs for their body size and body condition in order to compensate partially for this environmental constraint.     

Variation in reproductive traits in European passerines in relation to nesting site: allometric scaling to body weight or adaptive variation?

Summary The relationships between different reproductive traits and body weight, in relation to nesting site, were studied in European passerines. Body weight explains a significant proportion of the variance in clutch size, egg weight, clutch mass, and incubation period. Whereas clutch size decreases, the other three traits increase with body weight. Even though both clutch mass and clutch size are related to body size, for a given body weight, concealed nesters lay a larger clutch and a greater clutch mass than open-nesters.     

Maturational costs of reproduction due to clutch size and ontogenetic conflict as revealed in the invisible fraction

Reproduction is thought to entail costs, but assessing survival costs associated with maturation as organisms express reproductive genes for the first time is problematic because many will die prior to expressing a phenotype. We quantified selection acting on this invisible fraction by measuring selection on predicted breeding values for clutch size estimated from a multigenerational pedigree of side-blotched lizards in which clutch size was heritable (h2=0.25+/-0.04). The survival effects of predicted breeding values for clutch size during maturation, however, differed between males and females indicating ontogenetic conflict. Increased mortality during maturation was associated with lower predicted breeding values for clutch size for females, but higher predicted breeding values for males who do not produce a clutch. Genetic correlations between clutch size and male and female survival were consistent with calculated selection differentials. Experimental yolk removal did not affect progeny survival during maturation, indicating that selection on maturing progeny was not due to confounding yolk-volume maternal effects, and hormone manipulations confirmed clutch size as the target of viability selection during maturation. Such episodes of selection prior to phenotypic expression of the trait will have important consequences for the evolution of reproductive investment.     

Latitudinal variation in clutch size–lay date regressions in Tachycineta swallows: effects of food supply or demography?

In a study of almost 16 000 nest records from seven swallow species across the entire Western Hemisphere, clutch sizes decline with relative laying date in each population, but the slope of this decline grows steeper with increasing distance from the equator. Late‐laying birds at all latitudes lay clutches of similar sizes, suggesting that latitudinal differences may be driven primarily by earlier‐laying birds. Focused comparisons of site‐years in North America with qualitatively different food availability indicate that food supply significantly affects mean clutch size but not the clutch size–lay date regression. Other studies on the seasonality of swallow food also indicate that steeper clutch size–lay date declines in the North are not caused by steeper earlier food peaks there. The distribution of lay dates grows increasingly right‐skewed with increasing latitude. This variation in lay‐date distributions could be due to the predominance of higher quality, early‐laying (and large‐clutched) individuals among populations at higher latitudes, resulting from latitudinal variation in mortality rates and the intensity of sexual selection. Our results underscore the importance of studying clutch size and lay date in tandem and suggest new research into the causes of their joint geographic variation.     

Clutch-size adjustments and skew models: effects on reproductive partitioning and group stability

Reproductive skew theory seeks to integrate social and ecologicalfactors thought to influence the division of reproduction amonggroup-living animals. However, most reproductive skew modelsonly examine interactions between individuals of the same sex.Here, we suggest that females can influence group stabilityand conflict among males by modifying their clutch size andmay do so if they benefit from the presence of subordinate malehelpers or from reduced conflict. We develop 3 models, basedon concessions-based, restraint, and tug-of-war models, in whichfemale clutch size is variable and ask when females will increasetheir clutch size above that which would be optimal in the absenceof male–male conflict. In concessions-based and restraintmodels, females should increase clutch size above their optimaif the benefits of staying for subordinate males are relativelylow. Relatedness between males has no effect on clutch size.When females do increase clutch size, the division of reproductionbetween males is not influenced by relatedness and does notdiffer between restraint and concessions-based models. Bothof these predictions are in sharp contrast to previous models.In tug-of-war models, clutch size is strongly influenced byrelatedness between males, with the largest clutches, but thefewest surviving offspring, produced when males are unrelated.These 3 models demonstrate the importance of considering third-partyinterests in the decisions of group-living organisms.     

The relationship between introduced European Starlings and the reproductive activities of Mountain Bluebirds and Tree Swallows in British Columbia,Canada

The European Starling Sturnus vulgaris is an introduced species in North America and is an aggressive competitor for tree cavity nest‐sites. Starlings are commonly considered to influence nest‐site selection and reproductive success of native cavity‐nesting species negatively. We examined the relationship between Starling nest density and the fecundity of two native secondary cavity‐using passerines, Mountain Bluebird Sialia currucoides and Tree Swallow Tachycineta bicolor. We monitored a total of 622 nests (approximately equal numbers for each of the three species) in woodpecker‐excavated and naturally occurring cavities in 29 small forest groves in central British Columbia, Canada, between 2000 and 2009. The dimensions of cavities used and the timing of nest initiation overlapped for all species, although Starlings initiated clutches earliest. Mixed‐effects models were used to assess whether nest abundance, clutch size or nest success were affected directly by Starling nest abundance, or indirectly via a shift in cavity selection or timing of breeding. Starlings and Mountain Bluebirds showed inverse trends in nest abundance. Mountain Bluebird clutch sizes were smaller if they were initiated later in the breeding season. There was weak evidence that Tree Swallow clutch size decreased with cavity depth when Starling nests were abundant, and increased with cavity depth where there were few Starling nests. We conclude that despite the aggressive nature of this exotic cavity‐nester, the influence of Starlings on native secondary cavity‐nesting passerines is modest where cavities are abundant.     

HERITABILITY AND SELECTION ON CLUTCH SIZE IN DARWIN'S MEDIUM GROUND FINCHES (GEOSPIZA FORTIS)

I studied the causes of variation and selection on clutch size in a population of Darwin's Medium Ground Finches (Geospiza fortis) on Isla Daphne Major, using data collected over a nine-year period (1976–1984). Quantitative-genetic analyses were carried out using the first clutch laid by a female in a given year. I used both unadjusted clutch-size values and values adjusted for between-year differences in mean clutch size for repeatability and regression analyses. Repeatability of clutch size was small (≤8%) and nonsignificant in all cases. Sib-sib analyses and parent-offspring regressions gave no evidence of a significant additive genetic component to clutch-size variation. Slopes of mother-daughter regressions were actually negative, suggesting possible maternal effects of mother's clutch size on daughter's clutch size. There was a small positive relationship between female age and clutch size but no effect of male or female body size or of large-scale differences in habitat quality on clutch size. Selection on clutch size was generally directional and positive: in almost all years in which successful breeding occurred, large clutches tended to fledge more chicks and produce more young surviving to the following year, possibly because there was no trade-off between clutch size and the weights of individual chicks at fledging. Thus, sustained directional selection for large clutch size may have reduced additive genetic variation in clutch size to low levels in this population. The size of a female's clutch may be primarily determined by unidentified proximate environmental factors which vary from year to year, rather than by any long-term optimization of clutch size with respect to adult survival.     

FACTORS DETERMINING A CLUTCH SIZE REDUCTION IN CALIFORNIA GULLS (LARUS CALIFORNICUS): A MULTI-HYPOTHESIS APPROACH

In the thirty-five years since David Lack first highlighted the importance of clutch size, a large number of hypotheses have been proposed relating clutch size variation to various environmental and demographic factors. Despite a great deal of both empirical and theoretical work on clutch size, there has been very little effort to test many of the competing hypotheses in explaining a clutch size difference between two populations of the same species. I have taken the latter approach in an effort to explain a clutch size reduction in the California Gull (Larus californicus) population at Mono Lake, California. I compared the breeding biologies of the gulls at Mono Lake and at Great Salt Lake, Utah, collecting data for three breeding seasons at Mono Lake and one breeding season at Great Salt Lake. These data included measurements of the conditions of 60 adults, growth and mortality measurements for approximately 900 chicks, 4450 nest-hours of parental care observations, and the results of egg-removal experiments on 40 females. I tested seven hypotheses to explain the clutch size reduction: age structure, egg predation, bet-hedging, effort reallocation, most productive brood size, parental mortality, and pre-egg food limitation. Each of these hypotheses is described in detail in the introduction. The pre-egg food limitation hypothesis is best able to explain the clutch size reduction at Mono Lake, although the egg-removal experiments show that the resource limitation is relative and not absolute. Clutch size variation at each site need not be viewed as the result of fine-scaled evolutionary adjustment, although the general clutch size decision machinery is presumably molded by selection. Future research must focus on the details of this clutch size decision machinery and its application to the concept of reproductive effort.     

Evolution of clutch size in cavity-excavating birds: the nest site limitation hypothesis revisited

There are two major competing hypotheses for variation in clutch size among cavity-nesting species. The nest site limitation hypothesis postulates that nesting opportunities are more limited for weak excavators, which consequently invest more in each breeding attempt by laying larger clutches. Alternatively, clutch size may be determined by diet; the clutch sizes of strong excavators may be smaller because they are able to specialize on a more seasonally stable prey. We built a conceptual model that integrated hypotheses for interspecific variation in clutch size and tested it with comparative data on life-history traits of woodpeckers (Picidae) and nuthatches (Sittidae). In most analyses, diet explained more variation in clutch size among species than did propensity to excavate. Migratory status was positively associated with clutch size but was difficult to distinguish from diet since resident species consumed more bark beetles (a prey available in winter) and had smaller clutches than migratory species. The literature suggests that cavities are not limited in natural, old-growth forests. Although our data do not rule out nest site limitation, we conclude that annual stability of food resources has a larger impact on the evolution of clutch sizes in excavators than does limitation of nest sites.     

Squamate hatchling size and the evolutionary causes of negative offspring size allometry

Although fecundity selection is ubiquitous, in an overwhelming majority of animal lineages, small species produce smaller number of offspring per clutch. In this context, egg, hatchling and neonate sizes are absolutely larger, but smaller relative to adult body size in larger species. The evolutionary causes of this widespread phenomenon are not fully explored. The negative offspring size allometry can result from processes limiting maximal egg/offspring size forcing larger species to produce relatively smaller offspring (‘upper limit’), or from a limit on minimal egg/offspring size forcing smaller species to produce relatively larger offspring (‘lower limit’). Several reptile lineages have invariant clutch sizes, where females always lay either one or two eggs per clutch. These lineages offer an interesting perspective on the general evolutionary forces driving negative offspring size allometry, because an important selective factor, fecundity selection in a single clutch, is eliminated here. Under the upper limit hypotheses, large offspring should be selected against in lineages with invariant clutch sizes as well, and these lineages should therefore exhibit the same, or shallower, offspring size allometry as lineages with variable clutch size. On the other hand, the lower limit hypotheses would allow lineages with invariant clutch sizes to have steeper offspring size allometries. Using an extensive data set on the hatchling and female sizes of > 1800 species of squamates, we document that negative offspring size allometry is widespread in lizards and snakes with variable clutch sizes and that some lineages with invariant clutch sizes have unusually steep offspring size allometries. These findings suggest that the negative offspring size allometry is driven by a constraint on minimal offspring size, which scales with a negative allometry.     

TESTING MODELS OF FACULTATIVE SEX RATIO ADJUSTMENT IN THE POLLINATING FIG WASP PLATYSCAPA AWEKEI

Female hymenoptera are renowned for their ability to adjust offspring sex ratio to local mate competition. When two females share a patch, they frequently produce clutches that differ in size, the female with the larger clutch optimally producing a more female‐biased sex ratio and vice versa. Females can base their sex allocation on their own clutch size only (“self‐knowledge”) or on both females’ clutch sizes (“complete knowledge”). Few studies have genotyped offspring so that each mother's contribution can be considered separately while none has found that both sources of information are used simultaneously. We genotyped 2489 wasps from 28 figs and assigned their maternity to one of the two foundress females. We argue that likelihood is a very convenient method to compare alternative models, while fitness calculations help to appreciate the cost of maladaptation. We find that the pollinating fig wasp Platyscapa awekei simultaneously uses its own as well as the other females clutch size in allocating sex. Indeed, the complete knowledge model explains the data 36 times better than the self‐knowledge model. However, large clutches contained fewer males than the optimal predictions leading to a median selection coefficient of 0.01.     

Selection on plasticity of seasonal life-history traits using random regression mixed model analysis

Theory considers the covariation of seasonal life-history traits as an optimal reaction norm, implying that deviating from this reaction norm reduces fitness. However, the estimation of reaction-norm properties (i.e., elevation, linear slope, and higher order slope terms) and the selection on these is statistically challenging. We here advocate the use of random regression mixed models to estimate reaction-norm properties and the use of bivariate random regression to estimate selection on these properties within a single model. We illustrate the approach by random regression mixed models on 1115 observations of clutch sizes and laying dates of 361 female Ural owl Strix uralensis collected over 31 years to show that (1) there is variation across individuals in the slope of their clutch size-laying date relationship, and that (2) there is selection on the slope of the reaction norm between these two traits. Hence, natural selection potentially drives the negative covariance in clutch size and laying date in this species. The random-regression approach is hampered by inability to estimate nonlinear selection, but avoids a number of disadvantages (stats-on-stats, connecting reaction-norm properties to fitness). The approach is of value in describing and studying selection on behavioral reaction norms (behavioral syndromes) or life-history reaction norms. The approach can also be extended to consider the genetic underpinning of reaction-norm properties.     

宁波滑蜥两性异形和雌性繁殖

蜥蜴的雌性繁殖特征对理解两性异形的进化原因起着重要作用。于2011年4月在安徽滁州采集宁波滑蜥(Scincella modesta),定量研究该种形态特征的两性异形和雌性繁殖特征,检验成体形态特征两性异形与雌性繁殖的相关性。研究共采集43条(17♀♀,26♂♂)宁波滑蜥,雄性和雌性个体的最大体长分别为47.4 mm和46.6 mm。雌雄两性在体长和头宽上没有差异,而在腹长和头长上差异显著,雄性有较大的头长,雌性有较大的腹长。宁波滑蜥年产单窝卵。窝卵数和窝卵重与雌体体长及腹长呈正相关,卵重与雌体体长无相关性。窝卵数及卵重的变异系数分别为0.20和0.12。卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数来增加繁殖输出。这些结果表明,宁波滑蜥是雌雄个体大小同形的两性异形模式,性选择使得雄性有着较大的头长,以具有较高的交配成功率,生育力选择使得雌性有着较大的腹长,以具有较大的生育力和繁殖输出。