Intraspecific Variation In Egg Size Research Articles

Variation in egg size and offspring phenotype among and within seven Arctic charr morphs.

Maternal effects have the potential to alter early developmental processes of offspring and contribute to adaptive diversification. Egg size is a major contributor to offspring phenotype, which can influence developmental trajectories and potential resource use. However, to what extent intraspecific variation in egg size facilitates evolution of resource polymorphism is poorly understood. We studied multiple resource morphs of Icelandic Arctic charr, ranging from an anadromous morph—with a phenotype similar to the proposed ancestral phenotype—to sympatric morphs that vary in their degree of phenotypic divergence from the ancestral anadromous morph. We characterized variation in egg size and tested whether egg size influenced offspring phenotype at early life stages (i.e., timing of‐ and size at‐ hatching and first feeding [FF]). We predicted that egg size would differ among morphs and be less variable as morphs diverge away from the ancestral anadromous phenotype. We also predicted that egg size would correlate with offspring size and developmental timing. We found morphs had different egg size, developmental timing, and size at hatching and FF. Egg size increased as phenotypic proximity to the ancestral anadromous phenotype decreased, with larger eggs generally giving rise to larger offspring, especially at FF, but egg size had no effect on developmental rate. The interaction between egg size and the environment may have a profound impact on offspring fitness, where the resulting differences in early life‐history traits may act to initiate and/or maintain resource morphs diversification.

High within-clutch repeatability of eggshell phenotype in Barn Swallows despite less maculated last-laid eggs

Abstract Ecological and life-history variation and both interspecific and intraspecific brood parasitism contribute to diversity in egg phenotype within the same species. In this study, Barn Swallows (Hirundo rustica erythrogaster) laid eggs with high intraclutch repeatability in egg size, shape, and maculation. Despite this high intraclutch repeatability, last-laid eggs had consistently less of the eggshell covered in spots and fewer spots than earlier-laid eggs in the clutch. We examined sources of interclutch and intraclutch variation using both direct measurements and custom software (SpotEgg, NaturePatternMatch) that provide detailed information on egg characteristics, especially maculation measures. In addition to our main findings, maculation on different sides of the egg was highly repeatable; however, only shape, proportion of the eggshell maculated, and average spot size were repeatable between first and replacement clutches. Low intraclutch variation in maculation could allow females to recognize their clutch and this may be adaptive for colonial nesting species, such as the Barn Swallow. Characterizing intraspecific variation in egg size, shape, and maculation is the first step in understanding whether intraclutch variation is low enough—and interclutch variation high enough—such that eggs could serve as identity signals.

Corrigendum: Inter- and Intra-specific variation in egg size among reef fishes across the Isthmus of Panama

Corrigendum: Inter- and Intra-specific variation in egg size among reef fishes across the Isthmus of Panama

Seasonal differences in egg size in three species of crabs from a tropical upwelling zone

ABSTRACTEgg size and offspring size are fundamentally important aspects of the life histories of all animals. However the impact of environmental conditions on intraspecific variation in egg size of marine invertebrates is poorly documented. Here we followed three species of intertidal crabs Xanthodius sternberghii, Petrolisthes armatus and Clibanarius albidigitus to understand how seasonal environmental variation in temperature and salinity associated with seasonal upwelling impacts egg size. Ovigerous females of both P. armatus and C. albidigitus were found year round, while X. sternberghii has a limited reproductive season, with ovigerous females found only between November and February. In all three species more than half of the variation in egg size was attributable to variation among broods from different females. Eggs collected during the dry, upwelling season were significantly larger than those collected during the wet, non-upwelling season. Multiple regression analysis showed that average egg size from each brood was significantly negatively correlated with temperature for all three species. Egg size was also negatively correlated with salinity in P. armatus when we controlled for temperature. Overall these results support the idea that changes in environmental temperature caused by seasonal upwelling play a significant role in generating seasonal differences in egg size.

Landscape‐scale life‐history gradients in New Zealand freshwater fish

Summary Landscape‐scale clines in environmental parameters can lead to life‐history gradients. Study of interspecific life‐history differences can provide evidence of evolutionary adaptations in response to environmental cues, whereas examination of intraspecific life‐history variation can identify the ecological mechanisms driving trait evolution. We examined egg size and fecundity variation in three species of closely related freshwater fish (Galaxiidae) which occur across a habitat gradient in South Island, New Zealand. Inter‐population trait variation was assessed in the species with the widest distribution to investigate the ecological mechanisms driving egg size evolution. Substantial interspecific egg size and fecundity differences were observed. Galaxias paucispondylus, which generally occurs in high altitude headwater streams, showed an average egg size an order of magnitude larger, and fecundity an order of magnitude lower than G. brevipinnis, a species which rears in pelagic environments. Galaxias vulgaris, which rears fluvial environments but is generally distributed in lower catchment reaches than G. paucispondylus, showed intermediate fecundity and egg size traits. This interspecific trait variation is likely to be driven by differences in the larval rearing habitat, i.e. rearing in cold high altitude locations requires large well‐developed larvae (and therefore large eggs) but these come at the cost of maternal fecundity, whereas in rearing in warmer lower catchment watercourses, and pelagic habitats, does not require such large well‐developed larvae. Hence, fitness is maximised by progressively increasing fecundity by reducing egg size across this habitat cline. Life history‐habitat trends were repeated when intraspecific patterns in the widely distributed G. vulgaris were assessed, with population egg size increasing, and fecundity decreasing, in relation to a suite of interrelated environmental variables up an approximate altitudinal cline. The results highlight how inter‐ and intraspecific variation in egg size–fecundity trade‐offs in closely related species can interact to drive the evolution of landscape‐scale life‐history gradients. Egg size differences are likely to be driven by differences in the quality of the larval rearing habitat, i.e. rearing in a challenging habitat requires a larger egg whereas in relatively benign larval rearing habitat, fecundity can be maximised by reducing egg size. The interspecific variation observed provides evidence of trait adaptation in response to an environmental cue, while the intraspecific inter‐population differences indicate the potential ecological mechanisms driving trait evolution.

Revisiting Fisher: range size drives the correlation between variability and abundance of British bird eggs.

We evaluate the correlation between intraspecific variation in egg size and population size in breeding British birds. Using information on abundance, range occupancy, migration status and phylogenetic relationships among species, we show that a wider geographical distribution rather than larger population size per se best predicts egg size variability. A similar result applies to wing length variability. Results from a phylogenetic path analysis suggest that geographical variation is the most parsimonious causal explanation for high intraspecific variation in common species.

Inter- and Intra-specific variation in egg size among reef fishes across the Isthmus of Panama

Effects of planktonic food supplies and temperature on pelagic fish larvae are thought to be the primary environmental determinants of adaptive variation in egg size. Differences between the Atlantic and Pacific coasts of Panama in primary production (higher in the Pacific due to upwelling) and temperature (less seasonal in the non-upwelling Caribbean) allow testing such ideas. We compared the volumes, dry weights and energy content of eggs of 24 species of reef fishes from the two sides of the isthmus during the cool and warm seasons. Both egg volume and egg dry weight were good predictors of egg energy content among species, although not within species. Caribbean species produced larger eggs than their close relatives in the Pacific. In the Pacific, eggs were significantly larger during the cool upwelling season than during the warm, non-upwelling period, with a similar but weaker seasonal pattern evident in the Caribbean. The production of larger eggs in the low-productivity Caribbean is consistent with the hypothesis that species produce larger eggs and offspring when larval food supplies are lower. Parallel patterns of seasonal variation in eggs size and the greater strength of that relationship in the Pacific indicate that temperature drives seasonal variation in egg size within species. The decline in egg size with increasing temperature, a general pattern among ectotherms, may be a physiological side-effect, due to differing effects of temperature on various metabolic processes during oogenesis or on hormones that influence growth and reproduction. Alternatively, the seasonal pattern may be adaptive in these fishes, by affecting larval performance or maintaining a particular timeline of major events during embryonic development.

Temperature-mediated trade-offs and changes in life-history integration in two slipper limpets (Gastropoda: Calyptraeidae) with planktotrophic development

Intraspecific variation in egg size and hatching size, and the genetic and environmental trade-offs that contribute to variation, are the basis of the evolution of life histories. The present study examined both univariate and multivariate temperature-mediated plasticity of life-history traits, as well as temperature-mediated trade-offs in egg size and clutch size, in two planktotrophic species of marine slipper limpets, Crepidula. Previous work with two species of Crepidula with large eggs and lecithotrophic development has shown a significant effect of temperature on egg size and hatching size. To further examine the effect of temperature on egg size in Crepidula, the effects of temperature on egg size and hatching size, as well as the possible trade-offs with other the life-history features, were examined for two planktotrophic species: Crepidula incurva and Crepidula cf. marginalis. Fieldcollected juveniles were raised at 23 or 28 °C and egg size, hatching size, capsules/brood, eggs/capsule, time to hatch, interbrood interval, and final body weight were recorded. Consistent with results for the lecithotrophic Crepidula, egg size and hatching size decreased with temperature in the planktotrophic species. The affects of maternal identity and individual brood account for more than half of the intraspecific variation in egg size and hatching size. Temperature also showed a significant effect on reproductive rate, with time to hatch and interbrood interval both decreasing with increasing temperature. However, temperature had contrasting effects on the number of offspring. Crepidula cf. marginalis has significantly more eggs/capsule and therefore more eggs per brood at 28 °C compared to 23 °C, although capsules/brood did not vary with temperature. Crepidula incurva, on the other hand, produced significantly more capsules/brood and more eggs per brood at the lower temperature, whereas the number of eggs/capsule did not vary with temperature. The phenotypic variance‐covariance matrix of life-history variables showed a greater response to temperature in C. incurva than in C. cf. marginalis, and temperature induced trade-offs between offspring size and number differ between the species. These differences suggest that temperature changes as a result of seasonal upwelling along the coast of Panama will effect the reproduction and evolution of life histories of these two co-occurring species differently. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, , ••‐••. ADDITIONAL KEYWORDS: adaptive phenotypic plasticity ‐ phenotypic covariance ‐ P-matrix ‐ temperature-size rule.

Manipulating developmental stress reveals sex‐specific effects of egg size on offspring phenotype

The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings.

Temperature-mediated plasticity and genetic differentiation in egg size and hatching size among populations of Crepidula (Gastropoda: Calyptraeidae)

Offspring size is a key characteristic in life histories, reflecting maternal investment per offspring and, in marine invertebrates, being linked to mode of development. Few studies have focused explicitly on intraspecific variation and plasticity in developmental characteristics such as egg size and hatching size in marine invertebrates. We measured over 1000 eggs and hatchlings of the marine gastropods Crepidula atrasolea and Crepidula ustulatulina from two sites in Florida. A common-garden experiment showed that egg size and hatching size were larger at 23 °C than at 28 °C in both species. In C. ustulatulina, the species with significant genetic population structure in cytochrome oxidase I (COI), there was a significant effect of population: Eggs and hatchlings from the Atlantic population were smaller than those from the Gulf. The two populations also differed significantly in hatchling shape. Population effects were not significant in C. atrasolea, the species with little genetic population structure in COI, and were apparent through their marginal interaction with temperature. In both species, 60‐65% of the variation in egg size and hatching size was a result of variation among females and, in both species, the population from the Atlantic coast showed greater temperature-mediated plasticity than the population from the Gulf. These results demonstrate that genetic differentiation among populations, plastic responses to variation in environmental temperature, and differences between females all contribute significantly to intraspecific variation in egg size and hatching size. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 489‐499. ADDITIONAL KEYWORDS: evolution of development ‐ maternal effects ‐ offspring size ‐ phylogeography.

Egg Size as a Life History Character of Marine Invertebrates: Is It All It's Cracked Up to Be?

Egg size is one of the most important aspects of the life history of free-spawning marine organisms, and it is correlated with larval developmental mode and many other life-history characters. Egg size is simple to measure and data are available for a wide range of taxa, but we have a limited understanding of how large and small eggs differ in composition; size is not always the best measure of the characters under selection. Large eggs are generally considered to reflect increased maternal investment, but egg size alone can be a poor predictor of energetic content within and among taxa. We review techniques that have been used to measure the energetic content and biochemical makeup of invertebrate eggs and point out the strengths and difficulties associated with each. We also suggest a number of comparative and descriptive approaches to biochemical constituent analysis that would strengthen our understanding of how natural selection shapes oogenic strategies. Finally, we highlight recent empirical research on the intrinsic factors that drive intraspecific variation in egg size. We also highlight the relative paucity of these data in the literature and provide some suggestions for future research directions.

Optimal Egg Size in Marine Invertebrates: Theory and Phylogenetic Analysis of the Critical Relationship between Egg Size and Development Time in Echinoids.

Life-history models for marine invertebrate larvae generally predict a dichotomy in egg size in different species: eggs should be either minimal in size or large enough to support development fully without larval feeding. This prediction is contradicted, however, by the empirical observation of wide, continuous variation in egg size between these extremes. The prediction of dichotomy rests on the assumption of a negative linear relationship between egg size and development time. Here, I present a simple model in which development time is inversely proportional to egg size. Incorporating this relationship into an optimality model produces predictions of intermediate rather than extreme egg size. Modeled variations in mortality, food availability, fertilization rates, and temperature all produce continuous shifts in the value of the intermediate optimal size, in direct contrast to those produced by previous models, which predict shifts between two extreme optima. Empirical data on echinoid egg size and development time strongly support the model's assumption of an inverse proportional relationship between egg size and development time. A composite phylogeny is constructed of the 37 species for which egg size, development time, water temperature, and phylogenetic relatedness are known. Independent contrasts are made of the evolutionary changes in egg size and development time. This analysis indicates that evolutionary shifts in development time are correlated with the inversely proportional shifts in egg size assumed in the model. The assumption of a negative linear relationship used in previous models is rejected. This model provides a potential explanation for intraspecific variation in egg size along environmental gradients, sympatric differences in egg size among species, and biogeographic trends in egg size and development mode across taxa.

Composition of Wood Duck Eggs in Relation to Egg Size, Laying Sequence, and Skipped Days of Laying

-We collected 138 freshly laid Wood Duck (Aix sponsa) eggs from 13 nests to determine the effects of egg size, laying sequence, and skipped laying days on egg composition. All components except yolk ash and eggshell, both wet and dry, increased in direct proportion to fresh-egg mass. Egg size increased during the first half of laying and decreased thereafter. The effects of laying sequence were component-specific. Absolute levels of neutral lipids (comprising 65.6% of dry yolk) were near average until about 75% of the clutch was completed and then declined. Mass of albumen components tended to increase sharply with the first few eggs and then decrease as laying progressed. Fat indices (egg lipid/lean dryegg content) tended to be highest in the first 40% of the clutch. We interpret laying-sequence effects on egg composition as adaptations that enable female Wood Ducks to initiate incubation before clutch completion and still allow for synchronous hatching without compromising the hatching success of first-laid eggs. Hens frequently skipped a laying day between the penultimate and ultimate egg, which tended to increase the mass of the yolk component in last-laid eggs compared with those that were laid the day following the penultimate egg. Received 16 August 1996, accepted 19 February 1997. VARIATION IN AVIAN EGG SIZE is largely attributable to differences among species, and contrasting developmental modes dictate primary differences in constituent proportions (Ricklefs 1977, Carey et al. 1980, Sotherland and Rahn 1987). Egg size also varies considerably within species, typically varying more among than within clutches (Ricklefs 1984, Rohwer 1986, Hepp et al. 1987). Intraspecific variation in egg size is related to proximate factors such as laying date (Runde and Barrett 1981, Bancroft 1984), food supply (Horsfall 1984, Pierotti and Bellrose 1986), and age (Ryder 1975, Crawford 1980, Gratto et al. 1983). Such factors however, exercise their influence within the confines of a large heritable component of egg size (Ojanen et al. 1979, Van Noordwijk et al. 1980). Recent attention has been focused on intraspecific variation in the composition of eggs. As with egg size, egg composition typically varies more among than within clutches (Ricklefs 1984, Bancroft 1985, Alisauskas 1986, Hepp et al. 1987) and has been shown to vary with re' E-mail: kennamer@srel.edu 2 Present address: W1396 Stokdyk Ingelse Road, Oostburg, Wisconsin 53070, USA. 3Present address: National Park Service, Southeast Support Office, 100 Alabama Street Southwest, Atlanta, Georgia 30303, USA. spect to female quality in Wood Ducks (Aix sponsa) as indexed by post-laying body mass (Hepp et al. 1987). Egg composition, however, is not known to vary greatly due to other factors (e.g. clutch size; Rohwer 1986, Arnold et al. 1991; but see Owen and West 1988). Intraclutch variation in egg composition has received less attention (but see Nisbet 1978, Alisauskas and Ankney 1985, Rohwer 1986, Meathrel and Ryder 1987). Nest attentiveness in precocial waterfowl commonly increases through the laying period with persistent incubation beginning after the clutch has been completed (Caldwell and Cornwell 1975, Cooper 1978, Afton 1980, Kennamer et al. 1990). Despite up to four days of total asynchrony among eggs in experimentally manipulated Lesser Snow Goose (Chen caerulescens) clutches, hatching synchrony can still be achieved (Davies and Cooke 1983). Kennamer et al. (1990) documented 100% hatching success in a Wood Duck clutch with up to four days of natural cumulative asynchrony. Apparently, embryos communicate with one another to synchronize their hatching by adjusting developmental rates (Vince 1964, Ockleford and Vince 1985). Reasons for such a complicated incubation strategy in species that hatch synchronously may relate to a combination of egg-viability and nest-predation effects (Arnold et al. 1987, Flint et al. 1994). In any case, egg com-

Intra- and inter-individual variation in reproductive effort in captive-breeding zebra finches (Taeniopygia guttata)

Intraspecific variation in egg size, clutch size, and timing of laying was studied in captive-breeding zebra finches (Taeniopygia guttata) maintained under conditions of constant temperature, humidity, photoperiod (14 h light: 10 h dark), and ad libitum food supply. Individual variation was marked in the experimental population: egg size 0.915–1.342 g, clutch size 2–7 eggs, and laying interval 4–13 days; however, within individual females egg size (r = 0.742) and clutch size (r = 0.588) were highly repeatable between first and second clutches. Body condition explained only 8% of egg size variation, and clutch size and laying interval were independent of body condition. Clutch size was negatively related to laying interval: females laying later relative to pairing laid smaller clutches (b = −0.175 eggs/day). Body mass of breeding females decreased by 1.57 g (9% of initial mass) during laying of first clutches; mass loss was positively related to initial body condition (R2 = 27.8%) and total clutch mass (R2 = 7.6%). Mass loss was lower (0.47 g) during laying of second or replacement clutches than during laying of first clutches. Individual variation in reproductive effort in captive-breeding zebra finches is very similar to that in free-living avian populations. Laboratory studies on captive-breeding species can provide a valuable approach for the study of proximate physiological mechanisms underlying intraspecific variation in reproduction.

Relationships among Fresh Mass, Incubation Time, and Water Loss in Japanese Quail Eggs

Egg size is commonly assumed to increase the fitness value of hatchlings, and yet, most intraspecific variation in egg size appears to be highly heritable. Because traits strongly associated with fitness are expected to have low heritabilities, these two observations are not mutually compatable unless other factors act to offset the fitness value of large eggs. In this paper, we assess the influence of intraspecific egg-size variation on incubation periods and rates of egg water loss among Japanese Quail (Coturnix japonica) eggs. In contrast to interspecific studies of these relationships, we observed very low correlations between the logarithms of fresh egg mass and incubation time (r2 = 0.016, P = 0.01, n = 378) and between fresh egg mass and daily water loss (r2 = 0.028, P = 0.03, n = 163). Analysis of fresh eggs and newly hatched chicks confirmed that heavier eggs lost proportionately less water during incubation. These observations suggest that statistical relationships derived from interspecific comparisons of egg size and egg physiology are not generally applicable to studies of intraspecific egg-size variation.

The relationship among egg size, density and food level on larval development in the wood frog (Rana sylvatica)

Although inter- and intraspecific variation in egg size among amphibians has been well documented, the relationship between egg size and fitness remains unclear. Recent attempts to correlate egg size intraspecifically with larval developmental patterns have been equivocal. In this study the development of larvae derived from large eggs and small eggs, from a single population in Maryland were compared under a range of food levels and larval population densities. Both food level and density had significant effects on the length of the larval period and size at metamorphosis. However, the response among larvae derived from different egg sizes was not additive. At low densities and high food levels, larvae from small eggs had longer larval periods and a larger size at metamorphosis than larvae derived from large eggs. In contrast, at high densities larvae from small eggs had longer developmental periods but were smaller at metamorphosis than larvae from large eggs. In addition, larvae from small eggs were more sensitive to density irrespective of food level. These results suggest that optimal egg size is correlated with environmental factors, which may explain the maintenance of both geographic and within population variation in egg size commonly observed in amphibians.

Temporal and spatial variation in egg size of 13 Panamanian echinoids

Though egg size of marine invertebrates has received a great deal of theoretical attention, and though sea urchin eggs have been studied for nearly a century, practically no data on intraspecific variation of echinoid egg size exist. This study examines temporal variation in egg size of 10 species of regular and three species of irregular echinoids from either side of the Isthmus of Panama. Data on spatial variation in egg volume are also presented for eight of these species. In all species mean size of eggs from different females collected from the same locality on the same day were significantly different. Daily (within-month) variation in egg size was significant in three out of the five species for which sufficiently large samples were collected: Eucidaris tribuloides (Lamarck), Diadema antillarum Philippi, and Lytechinus variegatus (Lamarck). No significant differences between daily means of egg volume were evident in D. mexicanum A. Agassiz and in Echinometra viridis A. Agassiz. Monthly means of egg volume were significantly different in seven out of the 13 species studied: Lytechinus variegatus, L. williamsi Chesher, Tripneustes ventricosus (Lamarck), Echinometra viridis, E. vanbrunti A. Agassiz, Clypeaster rosaceus (Linnaeus), and C. subdepressus (Gray). Between-year variation was also significant in all of these species, except Lytechinus variegatus. All Caribbean species with significant monthly variation show a decline in egg size after September, but no obvious environmental fluctuation can be linked to this change. Echinometra lucunter (Linnaeus) showed no significant variation between months of the same year, but exhibited differences between years. No significant monthly or annual variation was observed in Eucidaris tribuloides, E. thouarsi (Valenciennes), Diadema antillarum, D. mexicanum, or Leodia sexiesperforata (Leske). When temporal variation at each locality was taken into account, only one species out of eight, Clypeaster subdepressus, showed spatial variation. Correlations between size of eggs collected at a particular time and the intensity of spawning by the population at that time were generally not significant, suggesting that size of mature eggs is not determined by reproductive state of the parental population. Correlations were also attempted (in three species of Echinometra) between egg size and body weight, gonadal content, and number of eggs carried by the mother. None of these variables was a good predictor of egg size. Only in E. viridis was there a significant correlation between egg size and gonadal content. Though its causes remain obscure, intraspecific variation in egg size found in these echinoids could be exploited to study the possible effects of this parameter on larval life history.