Effects of parental survival on clutch size decisions in fluctuating environments

Whereas in constant environments parental survival has no effect on optimal clutch size in the absence of trade-offs between juvenile and parental survival, the situation is drastically different in fluctuating environments. We consider a model in which, with respect to reproduction, parents and offspring are equivalent at the start of the next breeding season. When generations are non-overlapping, the clutch size maximizing geometric mean surviving number of offspring is optimal among all pure clutch size strategies. We prove that, as parental survival increases relative to that of the offspring, the optimal clutch size converges to the arithmetic mean maximizing clutch size (the so-called ‘Lack clutch size’). We also give a numerical procedure for calculating optimal mixed strategies and we show that, as environmental variance increases and/or parental survival decreases, mixed rather than pure strategies become optimal. Furthermore, we explain how to estimate fitness from empirical data under the assumptions of our model. This revised version was published online in July 2006 with corrections to the Cover Date.     

The association between the emergence of cooperative breeding and clutch size

Previous theoretical work has suggested that smaller brood sizes helped facilitate the emergence of cooperative breeding in birds. However, recent empirical evidence has found no statistically significant difference between the clutch sizes of cooperative breeders and that of noncooperative breeders. One explanation for this finding is that while small clutch sizes may predispose species to cooperative breeding, the emergence of cooperative breeding itself may influence the evolution of clutch size. Here, we develop a set of models using population dynamics to describe how the emergence of cooperative breeding influences clutch size. We find, in contrast to previous theoretical work, that the emergence of cooperative breeding does not necessarily decrease (and under certain conditions may actually increase) clutch size. In particular, clutch size may increase after the emergence of cooperative breeding if helpers – philopatric individuals that assist their breeding relatives – are able to substantially improve breeder fecundity at low costs to their own survival, and if the association between breeder and helper is brief. In many cases, clutch size increases following the emergence of cooperative breeding not because it is optimal for the breeder, but as the result of breeder–helper conflict over resource allocation.     

Sibling-size variation in brown trout Salmo trutta in relation to egg size and stream size

Sibling-size variation (SSV), estimated as the coefficient of variation of egg size, was investigated for 13 populations of brown trout Salmo trutta . SSV was negatively correlated with mean egg size both at the population and individual levels. After correction for the effect of mean egg size, SSV was also negatively correlated with stream size. These results provide new information about how salmonid SSV can vary at different ecological scales (individual, population and region). The results are discussed in light of competing theories for explaining SSV: (1) the passive effect hypothesis, stating that egg size variation follows passively from selection on egg size and (2) the bet-hedging hypothesis, stating that high SSV is adaptive in unpredictable environments.     

State-dependent life-history theory and its implications for optimal clutch size

Summary Life-history theory is usually based on an animal's age or size. McNamara describes a general technique for finding the optimal life-history when an organism's strategy is allowed to depend on other aspects of its state. In this paper we describe the technique in the context of previous work in life-history theory and discuss how it can be used to look at decisions on a finer time scale than the usual annual decisions. We show how it can be used to model optimal clutch size when there is a trade-off between number and quality of offspring. It is shown that the optimal clutch size is typically less than the most productive clutch size. Measuring the value of a clutch in terms of the number of offspring that survive to breed or even the number of grandchildren that survive to breed may give misleading results.     

Phenotypic plasticity in fluctuating environments: consequences of the lack of individual optimization

I consider the problem of characterizing the optimal plasticresponse when there are large-scale fluctuations in the environmentaffecting all population members. Individuals differ in theirstate, and each makes a reproductive decision before the environmentalconditions are known. An individual's state, its decision, andenvironmental conditions together determine the number of descendantsleft at the next decision epoch. I restrict attention to thesimple problem in which the state of the descendants left atthis epoch does not depend on these three factors. Because theenvironment is fluctuating, there is no individual optimization;instead the best action in one state implicitly depends on thebest action in other states. I characterize an optimal state-dependentstrategy, give a method of computation, and show how behaviorof each individual following the optimal strategy may be reinterpretedas a form of "individual optimization." Concepts are illustratedwith an example of optimal dutch size as a function of territoryquality.     

Elevational gradient in clutch size of Red‐faced Warblers

Our understanding of life history evolution has benefited from debates regarding the underlying causes, and geographic ubiquity, of spatial patterns in avian clutch sizes. Past studies have revealed that birds lay smaller clutch sizes at higher elevation. However, in most previous studies, investigators have failed to adequately control for elevational differences in breeding phenology. To better understand the elevational gradient in avian clutch size, we need to know how clutch size changes across the entire elevational breeding range of a species (i.e., the shape of the relationship between elevation and clutch size), and whether the elevational gradient in clutch size is merely an artifact of elevational gradients in breeding phenology or breeding season length. We examined the relationship between breeding elevation and clutch size of Red‐faced Warblers (Cardellina rubrifrons) along a 1000‐m elevational gradient in Arizona. Our objectives were to determine how clutch size changed with elevation, and if the relationship between clutch size and elevation merely reflected elevational changes in breeding season length or phenology. The proportion of 5‐egg clutches decreased and the proportion of 3‐ and 4‐egg clutches increased non‐linearly with increasing elevation, even after controlling for the elevational gradient in nest initiation date. Thus, average clutch size declined across the elevational breeding range of Red‐faced Warblers, but this decline was not due to elevational variation in breeding phenology. Timing of breeding changed, but the duration of the breeding season did not change appreciably across the elevational gradient. Hence, elevational differences in breeding season length or breeding phenology cannot explain why Red‐faced Warblers (and perhaps other birds) breeding at higher elevations have smaller clutches.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

Interspecific competition affects evolutionary links between cavity nesting,migration and clutch size in Old World flycatchers (Muscicapdae)

The ecology of cavity nesting in passerine birds has been studied extensively, yet there are no phylogenetic comparative studies that quantify differences in life history traits between cavity‐ and open‐nesting birds within a passerine family. We test existing hypotheses regarding the evolutionary significance of cavity nesting in the Old World flycatchers (Muscicapidae). We used a multi‐locus phylogeny of 252 species to reconstruct the evolutionary history of cavity nesting and to quantify correlations between nest types and life history traits. Within a phylogenetic generalized linear model framework, we found that cavity‐nesting species are larger than open‐nesting species and that maximum clutch sizes are larger in cavity‐nesting lineages. In addition to differences in life history traits between nest types, species that breed at higher latitudes have larger average and maximum clutch sizes and begin to breed later in the year. Gains and losses of migratory behaviour have occurred far more often in cavity‐nesting lineages than in open‐nesting taxa, suggesting that cavity nesting may have played a crucial role in the evolution of migratory behaviour. These findings identify important macro‐evolutionary links between the evolution of cavity nesting, clutch size, interspecific competition and migratory behaviour in a large clade of Old World songbirds.     

Biochemical and egg size evolution of freshwater fishes in the Rhinogobius brunneus complex (Pisces, Gobiidae) in Okinawa, Japan

Many colour morphs have been recognized in the Rhinogobius brunneus complex. A recent electrophoretic study has revealed that some of the colour morphs are well differentiated from each other genetically. In Okinawa, egg-size and life-history variation has been found in addition to the colour variation in this species complex. To clarify the nature of this life-history variation, gobies of a fluviatile morph with large eggs as well as three other amphidromous morphs with small eggs, inhabiting a single stream sympatrically in Okinawa, were analysed by electrophoresis and the females were also used for comparison of egg and clutch sizes. Electrophoretic data for 34 loci showed that each morph was separated by a fixed-allele difference for at least one locus, indicating that the four morphs which occurred sympatrically are reproductively isolated from each other. However, Nei's genetic distance between the fluviatile morph and one of the amphidromous morphs was much smaller (0.026) than distances among amphidromous gobies (0.323-0.480). Egg size of the former was by far the largest among the four. These results imply that speciation of the fluviatile morph accompanied by the egg-size increase has been completed rapidly without considerable genetic differentiation.     

Parasitoid clutch size and irreversible evolution

Previously, theoretical and empirical studies suggested that parasitoids developing in small multiple-egg broods would evolve siblicidal behaviour, making such brood sizes rare and single-egg broods an evolutionary absorbing state. Recent evidence, however, suggests that small gregarious broods are relatively stable in many parasitoid taxa, and that gregarious development has evolved many times from solitary development. This suggests that new research is needed to assess how nonsiblicidal behaviour can spread and become stable. We discuss some potentially rewarding possibilities.     

Experimental evolution of a more restrained clutch size when filial cannibalism is prevented in burying beetles Nicrophorus vespilloides

The overproduction of offspring is commonly associated with high hatching failure and a mechanism for dispensing with surplus young. We used experimental evolution of burying beetle populations Nicrophorus vespilloides to determine causality in these correlations. We asked does eliminating the mechanism for killing “spare” offspring cause the evolution of a more restrained clutch size and consequently select for reduced hatching failure? N. vespilloides typically overproduces eggs but kills 1^st instar larvae through partial filial cannibalism during brood care. We established replicate evolving populations that either could practice filial cannibalism (Full Care) or could not, by removing parents before their young hatched (No Care). After 20+ generations of experimental evolution, we measured clutch size and hatching success. We found that No Care females produced fewer eggs than Full Care females when allowed to breed on a small corpse, a finding not explained by differences in female quality. On larger corpses, females from both populations laid similar numbers of eggs. Furthermore, hatching success was greater in the No Care populations on small corpses. Our results suggest that the adaptive overproduction of offspring depends on a mechanism for eliminating surplus young and that killing offspring, in turn, relaxes selection against hatching failure.     

The demands of incubation and avian clutch size

We reviewed information on the demands of incubation to examine whether these could influence the optimal clutch size of birds. The results indicate that appreciable metabolic costs of incubation commonly exist, and that the incubation of enlarged clutches can impose penalties on birds. In 23 studies on 19 species, incubation metabolic rate (IMR) was not elevated above the metabolic rate of resting non-incubating birds (RMR), but contrary to the physiological predictions of King and others, IMR was greater than RMR in 15 studies on 15 species. Across species, IMR was substantially above basal metabolic rate (BMR), averaging 1.606 × BMR. Of six studies on three species performed under thermo-neutral conditions, none found IMR to be in excess of RMR. IMRs measured exclusively within the thermo-neutral zone averaged only 1.08 × BMR contrasting with the significantly higher figure of 1.72 × BMR under wider conditions. 16 of 17 studies on procellariiforms found IMR below RMR, indicating a significant difference between this and other orders. We could find no other taxonomic, or ecological factors which had clear effects on IMR. Where clutch size was adjusted experimentally during incubation, larger clutches were associated with: significantly lower percentage hatching success in 11 of 19 studies; longer incubation periods in eight of ten studies; greater loss of adult body condition in two of five studies; and higher adult energy expenditure in eight of nine studies. Given that incubation does involve metabolic costs and given that the demands of incubation increase sufficiently with clutch size to affect breeding performance, we propose that the optimal clutch size of birds may in part by shaped by the number of eggs the parents can afford to incubate.     

Sex in an uncertain world: environmental stochasticity helps restore competitive balance between sexually and asexually reproducing populations

Like many organisms, individuals of the freshwater ostracod species Eucypris virens exhibit either obligate sexual or asexual reproductive modes. Both types of individual routinely co‐occur, including in the same temporary freshwater pond (their natural habitat in which they undergo seasonal diapause). Given the well‐known two‐fold cost of sex, this begs the question of how sexually reproducing individuals are able to coexist with their asexual counterparts in spite of such overwhelming costs. Environmental stochasticity in the form of ‘false dawn’ inundations (where the first hydration is ephemeral and causes loss of early hatching individuals) may provide an advantage to the sexual subpopulation, which shows greater variation in hatching times following inundation. We explore the potential role of environmental stochasticity in this system using life‐history data analysis, climate data, and matrix projection models. In the absence of environmental stochasticity, the population growth rate is significantly lower in sexual subpopulations. Climate data reveal that ‘false dawn’ inundations are common. Using matrix projection modelling with and without environmental stochasticity, we demonstrate that this phenomenon can restore appreciable balance to the system, in terms of population growth rates. This provides support for the role of environmental stochasticity in helping to explain the maintenance of sex and the occurrence of geographical parthenogenesis.     

Amphicarpic plants: definition,ecology, geographic distribution,systematics, life history,evolution and use in agriculture

Although most plants produce all of their fruits (seeds) aboveground, amphicarpic species produce fruits (seeds) both above‐ and belowground. Our primary aims were to determine the number of reported amphicarpic species and their taxonomic, geographic, life form and phylogenetic distribution, to evaluate differences in the life history of plants derived from aerial and subterranean seeds, to discuss the ecological and evolutionary significance of amphicarpy, to explore the use of amphicarpic plants in agriculture, and to suggest future research directions for studies on amphicarpy. Amphicarpy occurs in at least 67 herbaceous species (31 in Fabaceae) in 39 genera and 13 families of angiosperms distributed in various geographical regions of the world and in various habitats. Seeds from aerial and subterranean fruits differ in size/mass, degree of dormancy, dispersal and ability to form a persistent seed bank, with aerial seeds generally being smaller, more dormant and more likely to be dispersed and to form a seed bank than subterranean seeds. In addition, plants produced by aerial and subterranean seeds may differ in survival and growth, competitive ability and biomass allocation to reproduction. Amphicarpic plants may exhibit a high degree of plasticity during reproduction. Subterranean fruits are usually formed earlier than aerial ones, and plants may produce only subterranean propagules under stressful environmental conditions. Differences in the life histories of plants from aerial and subterranean seeds may be an adaptive bet‐hedging strategy.     

Correlated evolution of colour pattern and body size in polymorphic pygmy grasshoppers, Tetrix undulata

Theory posits that selection on functionally interrelated characters will promote physical and genetic integration resulting in evolution of favourable trait-value combinations. The pygmy grasshopper Tetrix undulata (Orthoptera: Tetrigidae) displays a genetically encoded polymorphism for colour pattern. Colour morphs differ in several traits, including behaviours, thermal biology and body size. To examine if these size differences may reflect phenotypic plasticity of growth and development in response to temperature we used a split brood-design and reared hatchlings from mothers belonging to different morphs in different thermal environments (warm or cold) until maturity. We found that time to maturity was longer in the cold compared with the warm treatment. In the warm (but not in the cold) treatment time to maturity also varied among individuals born to mothers belonging to different colour morphs. Although low temperature and long development time are normally accompanied by increased body size in ectotherms, our results revealed no difference in size at maturity between individuals reared in the two temperature treatments. There was also an increase (not a decrease) in adult body size with shortened time to maturity across families within each treatment. Taken together, this suggests that body size is canalized against environmental perturbations, and that early maturation does not necessarily trade off against a size-mediated decrease in fecundity. Heritability of body size was moderate in magnitude. Moreover, body size at maturity varied among individuals belonging to different morphs and was influenced also by maternal colour morph, suggesting that a genetic correlation exists between colour pattern and body size. These findings suggest that different characters have evolved in concert and that the various colour morphs represent different evolutionary strategies, i.e., alternative peaks in a multi-modal adaptive landscape.     

On the evolution of clutch size and nest size in passerine birds

Summary I examined the hypothesis that the clutch size of some altricial birds may be limited by over-crowding of the nestlings in the nest, by comparing data on different species of European passerines. Large-sized birds build, relative to the body, larger nests than small-sized birds, both as regards the inner and the outer nest widths and as regards edge breadth; only inner nestcup depth did not change relatively to body size. Nest size also varied in relation to nesting place. Birds with open nests built off the ground had a rather narrow nestcup, whereas those with a domed nest, or which nest in a cavity, had a wide nestcup. When only open-nesters were compared, birds nesting on, or close to, the ground tended to have a wider nestcup than birds nesting above the ground. Inner nestcup width was correlated with the amount of mosses and lichens used in building the nest; the more of such materials the narrower the nestcup. The three variables: standardised body size, nesting place, and type of nesting material used accounted for 92% of the overall variation observed in inner nestcup width. When controlling for adult body size, clutch size was positively correlated with the size of the nestcup. A multiple regression analysis showed that relative nestcup depth, nest site, and type of nesting materials used, accounted for 64% of the overall variation in clutch size.     

Hatching plasticity in the tropical gastropod Nerita scabricosta

Hatching plasticity has been documented in diverse terrestrial and freshwater taxa, but in few marine invertebrates. Anecdotal observations over the last 80 years have suggested that intertidal neritid snails may produce encapsulated embryos able to significantly delay hatching. The cause for delays and the cues that trigger hatching are unknown, but temperature, salinity, and wave action have been suggested to play a role. We followed individual egg capsules of Nerita scabricosta in 16 tide pools to document the variation in natural time to hatching and to determine if large delays in hatching occur in the field. Hatching occurred after about 30 d and varied significantly among tide pools in the field. Average time to hatching in each pool was not correlated with presence of potential predators, temperature, salinity, or pool size. We also compared hatching time between egg capsules in the field to those kept in the laboratory at a constant temperature in motionless water, and to those kept in the laboratory with sudden daily water motion and temperature changes. There was no significant difference in the hatching rate between the two laboratory treatments, but capsules took, on average, twice as long to hatch in the laboratory as in the field. Observations of developing embryos showed that embryos in the field develop slowly and continuously until hatching, but embryos in the laboratory reach the hatching stage during the first month of development and remain in stasis after that. Instances of hatching plasticity in benthic marine invertebrates, like the one in N. scabricosta, could greatly enhance our ability to investigate the costs and benefits of benthic versus planktonic development, a long‐standing area of interest for invertebrate larval biologists.     

Offspring allocation in externally ovipositing fig wasps with varying clutch size and sex ratio

The simultaneous optimization of clutch size and sex ratio isa tricky problem. Unless parameters such as host size or fecundityexist to pin down the optimal clutch size, this problem remainselusive to analytical analysis. This is because the fitnesslandscape with respect to clutch size and sex ratio does nothave one single evolutionarily stable peak toward which thepopulation can evolve. To solve this problem, I used a computeremulation to optimize both clutch size and sex ratio using externallyovipositing fig wasps as a model taxon. The simulation approachallows the use of integer numbers of eggs rather than assumingthat females can produce any sex ratio between 0 and 1. Whenfemales have no information about the patches on which theyoviposit, they produce either large clutches with a strong femalebias or clutches of a single male egg. When females have completeknowledge of their oviposition site, a set of conditional substrategiesis evolutionarily stable. Again, these substrategies are eitherlarge clutches with a female bias or dutches consisting of asingle male egg. This dichotomous oviposition pattern resultsin unrelated males sharing a fig, a condition conducive to theevolution of fatal fighting. Selection on female ovipositionstrategies may therefore be an important driving force behindhigh levels of fighting observed between male fig wasps.