skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: The Evolution of Offspring Size: A Metabolic Scaling Perspective
Abstract Size at the start of life reflects the initial per offspring parental investment—including both the embryo and the nutrients supplied to it. Initial offspring size can vary substantially, both within and among species. Within species, increasing offspring size can enhance growth, reproduction, competitive ability, and reduce susceptibility to predation and starvation later in life, that can ultimately increase fitness. Previous work has suggested that the fitness benefits of larger offspring size may be driven by energy expenditure during development—or how offspring metabolic rate scales with offspring size. Despite the importance of early-life energy expenditure in shaping later life fitness trajectories, consideration of among-species scaling of metabolic rate at the time of birth as a potential source of general metabolic scaling patterns has been overlooked by theory. Here, we review the patterns and processes of energy expenditure at the start of life when mortality is often greatest. We compile existing data on metabolic rate and offspring size for 191 ectotherm species spanning eight phyla and use phylogenetically controlled methods to quantify among-species scaling patterns. Across a 109-fold mass range, we find that offspring metabolic rate scales hypometrically with size, with an overall scaling exponent of 0.66. This exponent varies across ontogenetic stage and feeding activity, but is consistently hypometric, including across environmental temperatures. Despite differences in parental investment, life history and habitat, large-offspring species use relatively less energy as a proportion of size, compared with small-offspring species. Greater residual energy can be used to fuel the next stages of life, particularly in low-resource environments. Based on available evidence, we conclude that, while large knowledge gaps remain, the evolution of offspring size is likely shaped by context-dependent selection acting on correlated traits, including metabolic rates maintaining hypometric scaling, which operates within broader physical constraints.  more » « less
Award ID(s):
2141592
PAR ID:
10402349
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Integrative and Comparative Biology
Volume:
62
Issue:
5
ISSN:
1540-7063
Page Range / eLocation ID:
1492 to 1502
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Seasonal changes in reproduction have been described for many taxa. As reproductive seasons progress, females often shift from greater energetic investment in many small offspring towards investing less total energy into fewer, better provisioned (i.e. larger) offspring. The underlying causes of this pattern have not been assessed in many systems.Two primary hypotheses have been proposed to explain these patterns. The first is an adaptive hypothesis from life‐history theory: early offspring have a survival advantage over those produced later. Accordingly, selection favours females that invest in offspring quantity early in the season and offspring quality later. The second hypothesis suggests these patterns are not intrinsic but result from passive responses to seasonal changes in the environment experienced by reproducing females (i.e. maternal environment).To disentangle the causes underlying this pattern, which has been reported in brown anole lizards (Anolis sagrei), we performed complementary field and laboratory studies. The laboratory study carefully controlled maternal environments and quantified reproductive patterns throughout the reproductive season for each female. The field study measured similar metrics from free ranging lizards across an entire reproductive season.In the laboratory, females increased relative effort per offspring as the reproductive season progressed; smaller eggs were laid earlier, larger eggs were laid later. Moreover, we observed significant among‐individual variation in seasonal changes in reproduction, which is necessary for traits to evolve via natural selection. Because these patterns consistently emerge under controlled laboratory conditions, they likely represent an intrinsic and potentially adaptive adjustment of reproductive effort as predicted by life‐history theory.The field study revealed similar trends, further suggesting that intrinsic patterns observed in the laboratory are strong enough to persist despite the environmental variability that characterizes natural habitats. The observed patterns are indicative of an adaptive seasonal shift in parental investment in response to a deteriorating offspring environment: allocating greater resources to late‐produced offspring likely enhances maternal fitness. 
    more » « less
  2. Synopsis New biophysical theory and electronic databases raise the prospect of deriving fundamental rules of life, a conceptual framework for how the structures and functions of molecules, cells, and individual organisms give rise to emergent patterns and processes of ecology, evolution, and biodiversity. This framework is very general, applying across taxa of animals from 10–10 g protists to 108 g whales, and across environments from deserts and abyssal depths to rain forests and coral reefs. It has several hallmarks: (1) Energy is the ultimate limiting resource for organisms and the currency of biological fitness. (2) Most organisms are nearly equally fit, because in each generation at steady state they transfer an equal quantity of energy (˜22.4 kJ/g) and biomass (˜1 g/g) to surviving offspring. This is the equal fitness paradigm (EFP). (3) The enormous diversity of life histories is due largely to variation in metabolic rates (e.g., energy uptake and expenditure via assimilation, respiration, and production) and biological times (e.g., generation time). As in standard allometric and metabolic theory, most physiological and life history traits scale approximately as quarter-power functions of body mass, m (rates as ∼m–1/4 and times as ∼m1/4), and as exponential functions of temperature. (4) Time is the fourth dimension of life. Generation time is the pace of life. (5) There is, however, considerable variation not accounted for by the above scalings and existing theories. Much of this “unexplained” variation is due to natural selection on life history traits to adapt the biological times of generations to the clock times of geochronological environmental cycles. (6) Most work on biological scaling and metabolic ecology has focused on respiration rate. The emerging synthesis applies conceptual foundations of energetics and the EFP to shift the focus to production rate and generation time. 
    more » « less
  3. Abstract Metabolic rate (MR) usually changes (scales) out of proportion to body mass (BM) as MR = aBMb, where a is a normalisation constant and b is the scaling exponent that reflects how steep this change is. This scaling relationship is fundamental to biology, but over a century of research has provided little consensus on the value of b, and why it appears to vary among taxa and taxonomic levels. By analysing published data on fish and taking an individual-based approach to metabolic scaling, I show that variation in growth of fish under naturally restricted food availability can explain variation in within-individual (ontogenetic) b for standard (maintenance) metabolic rate (SMR) of brown trout (Salmo trutta), with the fastest growers having the steepest metabolic scaling (b ≈ 1). Moreover, I show that within-individual b can vary much more widely than previously assumed from work on different individuals or different species, from –1 to 1 for SMR among individual brown trout. The negative scaling of SMR for some individuals was caused by reductions in metabolic rate in a food limited environment, likely to maintain positive growth. This resulted in a mean within-individual b for SMR that was significantly lower than the across-individual (“static”) b, a difference that also existed for another species, cunner (Tautogolabrus adspersus). Interestingly, the wide variation in ontogenetic b for SMR among individual brown trout did not exist for maximum (active) metabolic rate (MMR) of the same fish, showing that these two key metabolic traits (SMR and MMR) can scale independently of one another. I also show that across-species (“evolutionary”) b for SMR of 134 fishes is significantly steeper (b approaching 1) than the mean ontogenetic b for the brown trout and cunner. Based on these interesting findings, I hypothesise that evolutionary and static metabolic scaling can be systematically different from ontogenetic scaling, and that the steeper evolutionary than ontogenetic scaling for fishes arises as a by-product of natural selection for fast-growing individuals with steep metabolic scaling (b ≈ 1) early in life, where size-selective mortality is high for fishes. I support this by showing that b for SMR tends to increase with natural mortality rates of fish larvae within taxa. 
    more » « less
  4. ABSTRACT The gill surface area of aquatic ectotherms is thought to be closely linked to the ontogenetic scaling of metabolic rate, a relationship that is often used to explain and predict ecological patterns across species. However, there are surprisingly few within-species tests of whether metabolic rate and gill area scale similarly. We examined the relationship between oxygen supply (gill area) and demand (metabolic rate) by making paired estimates of gill area with resting and maximum metabolic rates across ontogeny in the relatively inactive California horn shark, Heterodontus francisci. We found that the allometric slope of resting metabolic rate was 0.966±0.058 (±95% CI), whereas that of maximum metabolic rate was somewhat steeper (1.073±0.040). We also discovered that the scaling of gill area shifted with ontogeny: the allometric slope of gill area was shallower in individuals <0.203 kg in body mass (0.564±0.261), but increased to 1.012±0.113 later in life. This appears to reflect changes in demand for gill-oxygen uptake during egg case development and immediately post hatch, whereas for most of ontogeny, gill area scales in between that of resting and maximum metabolic rate. These relationships differ from predictions of the gill oxygen limitation theory, which argues that the allometric scaling of gill area constrains metabolic processes. Thus, for the California horn shark, metabolic rate does not appear limited by theoretical surface-area-to-volume ratio constraints of gill area. These results highlight the importance of data from paired and size-matched individuals when comparing physiological scaling relationships. 
    more » « less
  5. Abstract Females and males can exhibit striking differences in body size, relative trait size, physiology, and behavior. As a consequence, the sexes can have very different rates of whole-body energy use, or converge on similar rates through different physiological mechanisms. Yet many studies that measure the relationship between metabolic rate and body size only pay attention to a single sex (more often males), or do not distinguish between sexes. We present four reasons why explicit attention to energy-use between the sexes can yield insight into the physiological mechanisms that shape broader patterns of metabolic scaling in nature. First, the sexes often differ considerably in their relative investment in reproduction, which shapes much of life-history and rates of energy use. Second, males and females share a majority of their genome but may experience different selective pressures. Sex-specific energy profiles can reveal how the energetic needs of individuals are met despite the challenge of within-species genetic constraints. Third, sexual selection often pushes growth and behavior to physiological extremes. Exaggerated sexually selected traits are often most prominent in one sex, can comprise up to 50% of body mass, and thus provide opportunities to uncover energetic constraints of trait growth and maintenance. Finally, sex-differences in behavior such as mating-displays, long-distance dispersal, and courtship can lead to drastically different energy allocation among the sexes; the physiology to support this behavior can shape patterns of metabolic scaling. The mechanisms underlying metabolic scaling in females, males, and hermaphroditic animals can provide opportunities to develop testable predictions that enhance our understanding of energetic scaling patterns in nature. 
    more » « less