Origin of evolutionary change in avian clutch size

Reproduction in a Northern Population of Clemmys guttata

For over a half century numerous hypotheses have surfaced aimed at explaining a key life history trait, the evolution of clutch size in birds. A principal goal has been to explain why clutch size generally increases with latitude both within species and among closely related species. Most hypotheses have stressed food limitation, predation, or seasonality. I present a novel hypothesis to explain geographic variation: a limitation of calcium resulting from broad scale variation in this element. Because the storage capacity of avian medullary bone is limited or nonexistent, during egg formation, female birds must intake supplemental calcium. Yet calcium and other exchangeable bases are much rarer in tropical soils. I briefly review the abundant experimental and observational evidence supporting how calcium limitation affects clutch size and other life history traits, and I present a series of predictions (and apparent support for them), stemming from the calcium variation and limitation hypothesis. The balance of evidence suggests that variability in availability of environmental calcium plays a proximate and ultimate role in the evolution of clutch size. Although this hypothesis is not mutually exclusive with others, it highlights another factor that needs to be considered in studies of the geographic variation in clutch size.

Animal species differ in the variability of their clutch sizes, as well as in mean clutch sizes. This phenomenon is particularly obvious in lizards, where virtually invariant clutch sizes have evolved independently in at least 23 lineages in seven families. Reduced variance in clutch size may arise either as an adaptation (because females with less variable clutch sizes have higher fitness) or as an indirect by-product of selection on other life-history characteristics. Comparative data on Australian scincid lizards indicate that variance in clutch sizes is lowest among species with low mean clutch sizes, small body sizes and a low variance in body sizes of adult females. Phylogenetic analysis shows that evolutionary decreases in the variance of clutch size have accompanied decreases in mean clutch sizes and decreases in the variance of adult female body sizes. Tropical lizards may also exhibit lower variance in clutch size. Most of these characteristics are correlated in occurrence, and may be allometrically tied to small body size. Hence, low variance in clutch size may be a consequence of allometric effects on a correlated suite of life-history characteristics. Exceptions to the general patterns noted above-especially, lizard species with invariant clutch sizes but large body sizes-may be due to loss of genetic variance for clutch sizes in lineages that have passed through a "bottleneck" of small body sizes and hence, low variance in clutch sizes.

Models predicting mechanisms driving sexual cannibalism in spiders with sexual size dimorphism (SSD) often assume that spiders use post‐copulatory food to channel nutrients into eggs and fecundity is altered through changes in clutch size or egg mass. I tested these assumptions using an orb web spider with extreme SSD,Argiope keyserlingi. I fed mated female spiders prey of either high protein‐low energy or low protein‐high energy composition. I measured egg energy density; a measure of the relative volumes of yolk and albumen. I predicted that ifA. keyserlingiincrease their egg energy density upon feeding on prey of a specific nutrient composition, they could enhance their fecundity by investing in more energy dense eggs. However, if the egg energy densities are dissimilar to their post‐copulatory prey they must be drawing energy from their somatic reserves to invest in eggs. In a further experiment I allowed female spiders to mate with and cannibalize males to determine if cannibalism induces similar effects on egg energy density. Male spider protein energy ratio was measured and found to resemble the high protein‐low energy prey. I found disagreement between the composition of post‐copulatory food and eggs in both experiments. Additionally, spiders fed high protein‐low energy prey lost weight indicating that they draw on their energy reserves to invest in eggs. I thus concluded that spiders that feed on high protein‐low energy prey or on males increase their egg energy density and, possibly, fecundity. However, the nutrient content of the prey or males cannot provide for investment in eggs. The energy invested in eggs is drawn from somatic reserves, probably induced by an as yet undescribed physiological trigger.

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.

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.

Geographic variation in reproduction in certain bird species has been explained in several ways. The larger clutch size at higher latitudes in several species of passerines in the northern regions of the Old World and New World (Lack 1947-48, 1968, Klomp 1970, Hussell 1972) has sometimes been accounted for by the extra hours of daylight for feeding activity by the parents at the higher latitudes (Lack 1947-48) and by the extra hazards faced by adult birds in more northern populations or by higher mortality of eggs and nestlings in the tropics (Skutch 1967). The short breeding season available to birds of the higher latitudes also may help explain the large clutch size of birds in those areas. With time for rearing no more than one brood, one adult may be likely to leave more offspring than another if it lays a large clutch. In more tropical areas the long nesting season, with repeated opportunities for rearing young e.g., Willis 1974) may provide an ecological setting where the long-term breeding success of a pair of birds is higher if little parental investment goes into a single nesting effort (Williams 1966). The numbers of eggs laid in a season and the number in each set or clutch within a season may vary in parasitic birds as well as in birds that rear their own young. Such variation may help provide a general explanation for the trends in the nesting passerines. Parasitic birds such as the cowbirds provide a natural experiment to test the generality of some of the explanations of variation in clutch size, particularly those explanations that are based on the concept that family size in birds has a selective history shaped mainly by the amount of food the parents can provide to their young. The brood parasites lay eggs in the nests of other species that rear their young. As they do not feed their own young, they may be expected to lay more eggs than their nesting relatives, and so to show a different pattern of geographic variation in breeding effort. To test the effectiveness of these general explanations in forecasting the reproductive variation of a parasitic bird, I sampled populations of Brown-headed Cowbirds (Molothrus ater) in Oklahoma, California, and Michigan. These areas differ in (a) latitude, (b) length of the breeding season, and (c) number of years the population has existed. The predictions were as follows: (1) if clutch is imite in birds by the amount of food the arents can find for their brood, then the n rth rn (Michigan) cowbirds should not hav lar er clutches than cowbirds in Oklahoma or California. (2) If clutch size is smaller than the number of young that parents usually can feed because long-term seasonal reproductive success is adversely affected by a big early reproductive effort (Williams 1966), then the northern (Michiga ) cowbirds should have larger clutches because they have a shorter breeding season, and hence should be less restrained in their

We examined reproduction over 3 yr using radio telemetry and X-rays in a South Carolina population of spotted turtles (Clemmys guttata). Spring courtship (March-April) coincided with aggregations of turtles; however, a second peak in courtship in the fall (September-October) did not coincide with such aggregations. Over 75% of the radio-tagged females were gravid in each year of the study. The nesting season lasted approximately two months (mid-May through mid-July). Nesting was primarily nocturnal, and most nests (17/21, 81%) were made in the woody debris of decaying logs and stumps. Incubation time (mean 5 79 d) decreased as nest temperature increased. Clutch size was not correlated to maternal body size, and we found no evidence for a tradeoff between clutch size and egg size. However, all measures of egg size and most measures of hatchling size were independent of maternal body size. We also compared reproduction among three widely separated populations of spotted turtles. Clutch size varied with latitude: clutch size was largest in the north (Ontario, mean 5 5.3 eggs), mid-sized in the central population (Pennsylvania, mean 5 3.9), and smallest in the south (South Carolina, mean 5 2.8). Variation in reproductive output among populations was attributable to both variation in number of eggs and to egg size. Most of this variation in clutch size and egg size was explained by differences in body size of females among populations. Because the spotted turtle is considered to be a Species at Risk throughout its range, the data provided in the current study will be useful in conservation planning and for directing future research on the reproductive ecology of freshwater turtles.

Data on clutch size and hatching success of P. expansa were gathered for seven beaches traditionally used by the species and re-analyzed statistically by means of regression analysis, of the number of eggs on the number of females (or nests) and of the number of young on the number of eggs. All regressions were linear, passed through the origin and had excellent fits. Average clutch size varied from 75 to 123, and presented geographic differentiation: (i) Rio Orinoco, (ii) Rio Trombetas + Rio Branco and (iii) Rio Juruá + Rio Purus. Average hatching success was ca. 83%. In P. unifilis there was also geographic variation in clutch size, the Iquitos area showing the highest values. Hatching success of P. unifilis was uniformly high: only one sample, from Iquitos, had less than 90% success. The outstanding fit of the clutch size regressions leads one to consider egg volume variability, which was found to be high in both species, in contradiction with current optimal egg size theory.

The majority of species in the scincid genus Emoia (Squamata: Scincidae) have a fixed clutch size of two eggs per clutch and produce between two and four clutches per year. One lineage within Emoia, the Emoia samoensis species group, consists of 13 species occurring in Melanesia and the islands of the southwestern Pacific Ocean, and exhibits variation in clutch size, with previously reported clutch sizes of two to five eggs. Little is known about reproduction in several members of this lineage including Emoia sanfordi, a large-bodied lizard endemic to the archipelago of Vanuatu in the South Pacific. We analyzed reproduction and clutch size in E. sanfordi females and discovered that there is a substantial amount of intraspecific variation, with clutch size ranging from two to seven eggs, with a modal clutch size of five eggs. Females were reproductively active throughout the study period of June through October and appear to be laying multiple clutches. The variation in clutch size seen in E. sanfordi is congruent with the variation previously reported within other closely related species.

Clutch size varies among individuals in most bird species. A widespread assumption is that such variation results from variable timing in the disruption of ovarian follicular growth that brings, with a few days' lag, egg‐laying to an end. Currently, there is empirical evidence that this is the case in Blue Tits Cyanistes caeruleus but not in Zebra Finches Taeniopygia guttata, in which the timing of follicular disruption has been shown to be invariant. Here, I investigate clutch size regulation of Common Swifts Apus apus. Using experimental egg removal, I show that, assuming the female gets enough egg contact, the determination of clutch size occurs at noon solar time on the day the first egg of a clutch is laid. In spite of individual variation in clutch size, there was no hint of any variability in the timing of clutch‐size determination. In this species therefore, the timing of the signal disrupting follicular growth appears invariant. The physiological mechanism that controls clutch size is discussed, including the existence of an endogenous circadian clock and potential zeitgeber, the developmental range of clutch size for the species, the sensory nature of the input that triggers follicular disruption, and the stress of laying extra eggs.

Clutch size in birds varies considerably among individuals within a population and within a given year. I consider three hypotheses which may account for the maintenance of this variation: (I) Individual optimization. Birds are assumed to adjust clutch size according to their ability to rear young. Those able to rear successfully a large clutch do so; those not so able, it is maintained, do best (with respect to fitness) by rearing a small clutch. The hypothesis views clutch size variation as a conditional evolutionarily stable strategy (ESS). (II) Tradeoff of clutch size and survival. Different clutch sizes produce equivalent “payoffs” (in terms of fitness) because of the tradeoff between clutch size and offspring survival and the tradeoff between clutch size and adult survival. The hypothesis posits a mixed ESS with respect to clutch size. (III) Year-to-year fluctuations in selection pressure. Selection favors different clutch sizes in different years; these fluctuations are essentially unpredictable. The population changes (genotypically) from year to year as a result of changes in the selection regime. The hypothesis does not posit evolutionary stability, i.e., populations are not in genetic equilibrium.

Maternal effects may strongly influence evolutionary response to natural selection but they have been little studied in the wild. We use a novel combination of experimental and statistical methods to estimate maternal effects on condition and clutch size in the collared flycatcher, where we define "condition" to be the nongenetic component of clutch size. We found evidence of two maternal effects. The first (m) was the negative effect of mother's clutch size on daughter's condition, when mother's condition was held constant. The second (M) was the positive effect of mother's condition on daughter's condition, when mother clutch size was held constant. These two effects oppose one another because mothers in good condition also lay many eggs. The maternal effects were large: Experimentally adding an egg to a mother's nest reduced clutch sizes of her daughters by 1/4 egg (i.e., m = -0.25). Measured degree of resemblance between mother and daughter clutch sizes yielded M = 0.43. The results weakly support the presence of heritable genetic variation in clutch size: additive genetic variance/total phenotypic variance = 0.33. This estimate was highly variable probably because, as we show, mother-daughter resemblance may depend hardly at all on the amount of genetic variance when maternal effects are present. Daughter-mother regression (a standard method for estimating heritability) is consequently a poor guide to the amount of genetic variance in clutch size. Our results emphasize the value of combining field experiments with observations for studying inheritance.

The evolution and regulation of clutch size has long been a central issue in ornithology. Early ornithologists realized that females of each species of bird lay a characteristic number of eggs, and we have been trying to determine ever since why this is so. In pursuit of the answer to this seemingly simple question, ornithologists have not only accumulated a wealth of egg data, but also have made important contributions to such diverse topics as life-history strategies, population regulation and group selection. Yet how clutch size is determined remains a controversial issue. The consensus that was once sought in the form of a central theory (Lack, 1968; Cody, 1966; Klomp, 1970; von Haartman, 1971) has disappeared in a sea of specific hypotheses. In this review we attempt to organize and summarize clutch size theories as they emerge in modified form from recent research and evaluate their ability to explain observed patterns in clutch size variation. We concentrate on the literature and concepts published since the review of Klomp (1970), but we incorporate earlier work when necessary.

Clutch size is an important determinant of female reproductive success in reptiles. Although female body size explains much variation in clutch size, other important factors include differences in food availability, predation risk, morphology, and demography. Ornate tree lizards, Urosaurus ornatus, display extensive variation in life history traits, including clutch size. Tree lizards primarily use 2 distinct habitat types—trees and rock surfaces—which influence both the performance and morphology of this species and may affect life history traits such as clutch size. As food availability, microclimate, and, potentially, predator escape probabilities differ between these 2 habitats, I predicted that tree- and rockdwelling lizards would allocate resources toward clutch size differently. Clutch size variation was compared among 15 populations of U. ornatus sampled from the different habitat types. Urosaurus ornatus individuals living on trees had significantly larger clutches than those living on rocks, even after including the effects of body size and environment. Two potential mechanisms leading to larger clutches in tree-dwelling lizards are (1) differences in food availability and (2) differences in performance (sprint vs. endurance) requirements for predator escape in the 2 habitats. Inconsistent distribution of habitat type across the phylogenetic tree indicates either many cases of independent evolution in the allocation strategies of these lizards or a consistent phenotypically plastic response to similar environmental challenges in different populations.