Repeatability and heritability of reproductive traits in free-ranging snakes

The underlying genetic basis of life-history traits in free-ranging animals is critical to the effects of selection on such traits, but logistical constraints mean that such data are rarely available. Our long-term ecological studies on free-ranging oviparous snakes (keelbacks, Tropidonophis mairii (Gray, 1841), Colubridae) on an Australian floodplain provide the first such data for any tropical reptile. All size-corrected reproductive traits (egg mass, clutch size, clutch mass and post-partum maternal mass) were moderately repeatable between pairs of clutches produced by 69 female snakes after intervals of 49-1152 days, perhaps because maternal body condition was similar between clutches. Parent-offspring regression of reproductive traits of 59 pairs of mothers and daughters revealed high heritability for egg mass (h2= 0.73, SE=0.24), whereas heritability for the other three traits was low (< 0.37). The estimated heritability of egg mass may be inflated by maternal effects such as differential allocation of yolk steroids to different-sized eggs. High heritability of egg size may be maintained (rather than eroded by stabilizing selection) because selection acts on a trait (hatchling size) that is determined by the interaction between egg size and incubation substrate rather than by egg size alone. Variation in clutch size was mainly because of environmental factors (h2=0.04), indicating that one component of the trade-off between egg size and clutch size is under much tighter genetic control than the other. Thus, the phenotypic trade-off between egg size and egg number in keelback snakes occurs because each female snake must allocate a finite amount of energy into eggs of a genetically determined size.     

Interspecific pairwise relationships among body size, clutch size and latitude: deconstructing a macroecological triangle in birds

Aim Ecogeographical ‘rules’, large‐scale patterns in ecological variables across geographical space, can provide important insights into the mechanisms of evolution and ecological assembly. However, interactions between rules could obscure both the observation of large‐scale patterns and their interpretation. Here, we examine a system of three variables interrelated by ecogeographical rules – the latitudinal increase in body size within closely related homeotherms (Bergmann’s rule), the negative allometry of clutch size (Calder’s rule) and the latitudinal increase in clutch size (Lack’s rule) – in a global dataset of birds. Location Global. Methods We used linear regressions and meta‐analysis techniques to quantify the three rules across clades and through the taxonomic hierarchy. Path analysis was used to quantify interactions between rules at multiple taxonomic levels, as a function of both phylogenetic inheritance of traits and indirect feedbacks between the three rules. Independent contrasts analyses were performed on four clades with available phylogenies, and the taxonomic partitioning of variation in each trait was quantified. Results Standardizing across all clades, Lack’s and Bergmann’s rules were supported at all taxonomic levels, with Calder’s rule being supported at the order level. Lack’s rule was consistently stronger and more often detected than the other two rules. Path analysis showed that the indirect effects often outweighed the direct effects of Calder’s rule at the genus level and Bergmann’s rule at the order level. Strong interactions between Calder’s and Bergmann’s rules led to a trade‐off between the rules depending on taxonomic resolution. Main conclusions We found strong interactions between Bergmann’s, Lack’s and Calder’s rules in birds, and these interactions varied in strength and direction over the taxonomic hierarchy and among avian clades. Ecogeographical rules may be masked by feedbacks from other, correlated variables, even when the underlying selective mechanism is operating. The apparently conflicting pairwise relationships among clutch size, body size and latitude illustrate the difficulty of interpreting individual pairwise correlations without recognition of interdependence with other variables.     

Reproductive allometry and the size-number trade-off for lizards

Fundamental to life-history theory is the assumed inverse proportionality between the number of offspring and the resource allocation per offspring. Lizards have been model organisms for empirical tests of this theory for decades; however, the expected negative relationship between clutch size and offspring size is often not detected. Here we use the approach developed by Charnov and Ernest to demonstrate that this often concealed trade-off can be made apparent in an interspecific comparison by correcting for size-dependent resource allocation. Our data set also shows a tight allometry for annual production that is consistent with life-history models for indeterminate growers. To account for nonindependence of species data we also compare the fit of nonphylogenetic and phylogenetic regression models to test for phylogenetic signal in these allometry and trade-off patterns. When combined, these results demonstrate that the offspring size/clutch size trade-off is not isolated to a single clutch but is shaped by the resource investment made over an entire year. We conclude that, across diverse lizard species, there is strong evidence for the predicted trade-off between offspring size and the annual number of eggs produced.     

Morphological correlates of life‐history variation: is lizard clutch size related to the number of germinal beds in the ovary?

Clutch size varies widely in reptiles, both intraspecifically and interspecifically. The mechanisms that generate this variation have attracted detailed study, focusing primarily on ecological factors (e.g. food availability), trade‐offs with other traits (e.g. offspring size), and physical constraints (e.g. maternal body shape). Does ovarian morphology, specifically the number of germinal beds from which ova are produced, also correlate with clutch size? Our review of published data on 58 lizard species reveals that clutch size is correlated with the number of germinal beds per ovary (more fecund species have more germinal beds), and that phylogenetic changes in germinal beds have been consistently associated with concurrent phylogenetic changes in fecundity. These correlations imply a causal connection: either clutch size is constrained by ovarian morphology, and/or ovarian morphology evolves to allow adaptive shifts in clutch size. The latter hypothesis is more consistent with available data. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 81–88.     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

Accounting for the causal basis of collinearity when measuring the effects of habitat loss versus habitat fragmentation

Collinearity among metrics of habitat loss and habitat fragmentation is typically treated as a nuisance in landscape ecology, and it is the norm to use statistical approaches that remove collinear information prior to estimating model parameters. However, collinearity may arise from causal relationships among landscape metrics and may therefore signal the occurrence of indirect effects (where one model predictor influences the response variable by driving changes in another influential predictor). Here we suggest that, far from being merely a statistical nuisance, collinearity may be crucial for accurately quantifying the effects of habitat loss versus habitat fragmentation. We use simulation modelling to create datasets of collinear landscape metrics in which collinearity arose from causal relationships, then test the ability of two statistical approaches to estimate the effects of these metrics on a simulated response variable: 1) multiple regression, which statistically removes collinearity, and was identified in a recent study as the best approach for estimating the effects of collinear landscape metrics (although this study did not account for any indirect effects implied by collinearity among metrics); and 2) path analysis, which accounts for the causal basis of collinearity. In agreement with this previous study, we found that multiple regression gave unbiased estimates of direct effects (effects not mediated by other model predictors). However, it gave biased estimates of total (direct + indirect) effects when indirect effects occurred. In contrast, path analysis reliably identified the causal basis of collinearity and gave unbiased estimates of direct, indirect, and total effects. We suggest that effective research on the impacts of habitat loss versus fragmentation will often require tools that can empirically test whether collinear landscape metrics are causally related, and if so, account for the indirect effects that these causal relationships imply. Path analysis, but not multiple regression, provides such a tool.     

Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models

Key life history traits such as breeding time and clutch size are frequently both heritable and under directional selection, yet many studies fail to document microevolutionary responses. One general explanation is that selection estimates are biased by the omission of correlated traits that have causal effects on fitness, but few valid tests of this exist. Here, we show, using a quantitative genetic framework and six decades of life‐history data on two free‐living populations of great tits Parus major, that selection estimates for egg‐laying date and clutch size are relatively unbiased. Predicted responses to selection based on the Robertson–Price Identity were similar to those based on the multivariate breeder's equation (MVBE), indicating that unmeasured covarying traits were not missing from the analysis. Changing patterns of phenotypic selection on these traits (for laying date, linked to climate change) therefore reflect changing selection on breeding values, and genetic constraints appear not to limit their independent evolution. Quantitative genetic analysis of correlational data from pedigreed populations can be a valuable complement to experimental approaches to help identify whether apparent associations between traits and fitness are biased by missing traits, and to parse the roles of direct versus indirect selection across a range of environments.     

Reduction in locomotor ability as a cost of reproduction in gravid snakes

Summary Recent studies suggest that lower survival among gravid squamate reptiles may be partially the result of decreased locomotor ability during gestation. In this study, we compared the speed and endurance of female garter snakes (Thamnophis marcianus), before, during, and after pregnancy. Gravid snakes had significantly lower locomotor performance than did non-gravid females, and performance varied among stages of gestation, reaching a minimum 0–6 weeks prior to parturition. Both number of offspring and relative clutch mass were inversely correlated with locomotor performance; as females increased these traits, locomotor ability decreased. If reduced locomotor performance results in greater risk of predation and/or lowered foraging ability, then natural selection (operating via differential mortality or feeding rates of gravid females) may result in important constraints on both clutch size and relative clutch mass in squamates.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Comparative statics of joint reproductive allocation

We perform a perturbation analysis (comparative statics) of how optimal reproductive effort and per offspring investment are jointly affected by different selective factors. The factors considered are: (1) mortality sources, classified according to affected stage (juvenile or adult) and to its nature (avoidable or unavoidable), and (2) resource (energy) availability for the adult individual. The joint approach reveals both direct and indirect effects of each selective pressure. These interactive effects spring from the nonlinearity of reproductive expenditure, separated into a part devoted to endowing offspring (provisioning cost) and another part invested to make reproduction possible (requisite cost). The latter is envisioned as a reverse sigmoid function of fecundity (most models, so far, have considered only the first kind of cost). The indirect effects have the consequence of enlarging the class of selective pressures that can induce changes of offspring size and clutch size, as compared with current explanations. So, they illuminate new causes for some effects, and show new effects for some well-known selective causes. Several joint patterns in the two variables, shown by animals and plants in the field, can thus be given more appropriate interpretations than traditional, piecewise, ones.     

Direct and indirect effects of environmental temperature on the evolution of reproductive strategies: an information-theoretic approach

For ectotherms, environmental temperature affects the optimal size and number of offspring via multiple mechanisms. First, temperature influences the performance of offspring, which directly affects the optimal size of offspring. Second, temperature influences maternal body size, which indirectly affects the optimal size and/or number of offspring when larger females acquire more energetic resources or provide better parental care. Although traditional statistical approaches might distinguish the relative importance of these effects, an information-theoretic approach enables one to estimate effects more accurately by identifying the best evolutionary model in a set of candidate models. Here, we use the Akaike Information Criterion to calculate the likelihoods of seven path models, each derived from one or more optimality models of reproduction. Variation in reproductive traits among populations of lizards (Sceloporus undulatus) was used to quantify support for the models. Our results overwhelmingly supported a model based on an indirect effect of temperature that is mediated by maternal size. Path coefficients of this model were consistent with the hypotheses that, first, larger females can acquire more energy for reproduction and, second, the survival of offspring depends on both their size and their density. Our analyses exemplify how information theory can identify evolutionary hypotheses that merit experimental testing.     

A neglected life-history trait: clutch-size variance in snakes

Most analyses of life-history traits have focused on mean values rather than their associated variance. We review published and original data on snakes, including records gathered over many years on single populations, to examine patterns in clutch-size variability in these animals. Within single populations, the coefficient of variation of clutch size did not vary significantly with maternal body size, or among years. The stability of clutch-size variance through time is consistent with experimental studies showing no significant influence of food intake rates on this characteristic. Clutch-size variances did not differ between viviparous and oviparous snakes, but were dependent upon allometric relationships involving maternal body size and the relationship between clutch size and body size. Clutch-size variability was highest in species with relatively variable female sizes, and with a high rate of increase in clutch size with increasing body size. These two factors acted to magnify the extent of clutch-size variability engendered by variability in maternal body sizes. The relationships among these variables were similar in the two squamate Suborders, but the larger body sizes and mean clutch sizes of snakes resulted in clutch-size variances being higher in snakes than in lizards.     

Life-history evolution on tropidurinae lizards: influence of lineage, body size and climate

The study of life history variation is central to the evolutionary theory. In many ectothermic lineages, including lizards, life history traits are plastic and relate to several sources of variation including body size, which is both a factor and a life history trait likely to modulate reproductive parameters. Larger species within a lineage, for example tend to be more fecund and have larger clutch size, but clutch size may also be influenced by climate, independently of body size. Thus, the study of climatic effects on lizard fecundity is mandatory on the current scenario of global climatic change. We asked how body and clutch size have responded to climate through time in a group of tropical lizards, the Tropidurinae, and how these two variables relate to each other. We used both traditional and phylogenetic comparative methods. Body and clutch size are variable within Tropidurinae, and both traits are influenced by phylogenetic position. Across the lineage, species which evolved larger size produce more eggs and neither trait is influenced by temperature components. A climatic component of precipitation, however, relates to larger female body size, and therefore seems to exert an indirect relationship on clutch size. This effect of precipitation on body size is likely a correlate of primary production. A decrease in fecundity is expected for Tropidurinae species on continental landmasses, which are predicted to undergo a decrease in summer rainfall.     

Egg size and offspring quality: a meta‐analysis in birds

Parents affect offspring fitness by propagule size and quality, selection of oviposition site, quality of incubation, feeding of dependent young, and their defence against predators and parasites. Despite many case studies on each of these topics, this knowledge has not been rigorously integrated into individual parental care traits for any taxon. Consequently, we lack a comprehensive, quantitative assessment of how parental care modifies offspring phenotypes. This meta‐analysis of 283 studies with 1805 correlations between egg size and offspring quality in birds is intended to fill this gap. The large sample size enabled testing of how the magnitude of the relationship between egg size and offspring quality depends on a number of variables. Egg size was positively related to nearly all studied offspring traits across all stages of the offspring life cycle. Not surprisingly, the relationship was strongest at hatching but persisted until the post‐fledging stage. Morphological traits were the most closely related to egg size but significant relationships were also found with hatching success, chick survival, and growth rate. Non‐significant effect sizes were found for egg fertility, chick immunity, behaviour, and life‐history or sexual traits. Effect size did not depend on whether chicks were raised by their natural parents or were cross‐fostered to other territories. Effect size did not depend on species‐specific traits such as developmental mode, clutch size, and relative size of the egg, but was larger if tested in captive compared to wild populations and between rather than within broods. In sum, published studies support the view that egg size affects juvenile survival. There are very few studies that tested the relationship between egg size and the fecundity component of offspring fitness, and no studies on offspring survival as adults or on global fitness. More data are also needed for the relationships between egg size and offspring behavioural and physiological traits. It remains to be established whether the relationship between egg size and offspring performance depends on the quality of the offspring environment. Positive effect sizes found in this study are likely to be driven by a causal effect of egg size on offspring quality. However, more studies that control for potential confounding effects of parental post‐hatching care, genes, and egg composition are needed to establish firmly this causal link.     

Latitudinal gradients in abundance, and the causes of rarity in the tropics: a test using Australian honeyeaters (Aves: Meliphagidae)

Several studies have uncovered interspecific latitudinal gradients in abundance (population density) such that tropical species tend to be, on average, less abundant than species at higher latitudes. The causes of this relationship remain poorly studied, in contrast to the relative wealth of literature examining the relationship to latitude of other variables such as range size and body mass. We used a cross-species phylogenetic comparative approach and a spatial approach to examine three potential determining factors (distribution, reproductive output and climate) that might explain why abundance correlates with latitude, using data from 54 species of honeyeaters (Meliphagidae) in woodland environments in eastern Australia. There is a strong positive correlation between mean abundance and latitude in these birds. Reproductive output (clutch size) was positively linked to both abundance and latitude, but partial correlation analysis revealed that clutch size is not related to abundance once the effects of latitude are removed. A subsequent multiple regression model that also considered range size, clutch size and body mass showed that latitude is the only strong predictor of abundance in honeyeaters. In the separate spatial analysis, the climatic variables that we considered (temperature, rainfall and seasonality) were all strongly linked to latitude, but none served as a better predictor of abundance than latitude per se, either individually or collectively. The most intriguing result of our analyses was that the cross-species latitudinal pattern in abundance was not evident within species. This suggests an intrinsic cause of the pattern of ‘rarity in the tropics’ in Australian honeyeaters. We suggest that evolutionary age may provide a key to understanding patterns of abundance in these birds.Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .     

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.     

WHY ARE CLUTCH SIZES MORE VARIABLE IN SOME SPECIES THAN IN OTHERS?

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.     

The Worldwide Variation in Avian Clutch Size across Species and Space

Traits such as clutch size vary markedly across species and environmental gradients but have usually been investigated from either a comparative or a geographic perspective, respectively. We analyzed the global variation in clutch size across 5,290 bird species, excluding brood parasites and pelagic species. We integrated intrinsic (morphological, behavioural), extrinsic (environmental), and phylogenetic effects in a combined model that predicts up to 68% of the interspecific variation in clutch size. We then applied the same species-level model to predict mean clutch size across 2,521 assemblages worldwide and found that it explains the observed eco-geographic pattern very well. Clutches are consistently largest in cavity nesters and in species occupying seasonal environments, highlighting the importance of offspring and adult mortality that is jointly expressed in intrinsic and extrinsic correlates. The findings offer a conceptual bridge between macroecology and comparative biology and provide a global and integrative understanding of the eco-geographic and cross-species variation in a core life-history trait.     

Life-history and ecological correlates of geographic variation in egg and clutch mass among passerine species

Broad geographic patterns in egg and clutch mass are poorly described, and potential causes of variation remain largely unexamined. We describe interspecific variation in avian egg and clutch mass within and among diverse geographic regions and explore hypotheses related to allometry, clutch size, nest predation, adult mortality, and parental care as correlates and possible explanations of variation. We studied 74 species of Passeriformes at four latitudes on three continents: the north temperate United States, tropical Venezuela, subtropical Argentina, and south temperate South Africa. Egg and clutch mass increased with adult body mass in all locations, but differed among locations for the same body mass, demonstrating that egg and clutch mass have evolved to some extent independent of body mass among regions. A major portion of egg mass variation was explained by an inverse relationship with clutch size within and among regions, as predicted by life-history theory. However, clutch size did not explain all geographic differences in egg mass; eggs were smallest in South Africa despite small clutch sizes. These small eggs might be explained by high nest predation rates in South Africa; life-history theory predicts reduced reproductive effort under high risk of offspring mortality. This prediction was supported for clutch mass, which was inversely related to nest predation but not for egg mass. Nevertheless, clutch mass variation was not fully explained by nest predation, possibly reflecting interacting effects of adult mortality. Tests of the possible effects of nest predation on egg mass were compromised by limited power and by counterposing direct and indirect effects. Finally, components of parental investment, defined as effort per offspring, might be expected to positively coevolve. Indeed, egg mass, but not clutch mass, was greater in species that shared incubation by males and females compared with species in which only females incubate eggs. However, egg and clutch mass were not related to effort of parental care as measured by incubation attentiveness. Ecological and life-history correlates of egg and clutch mass variation found here follow from theory, but possible evolutionary causes deserve further study.