Egg Size Effects across Multiple Life-History Stages in the Marine Annelid Hydroides diramphus

The optimal balance of reproductive effort between offspring size and number depends on the fitness of offspring size in a particular environment. The variable environments offspring experience, both among and within life-history stages, are likely to alter the offspring size/fitness relationship and favor different offspring sizes. Hence, the many environments experienced throughout complex life-histories present mothers with a significant challenge to optimally allocate their reproductive effort. In a marine annelid, we tested the relationship between egg size and performance across multiple life-history stages, including: fertilization, larval development, and post-metamorphosis survival and size in the field. We found evidence of conflicting effects of egg size on performance: larger eggs had higher fertilization under sperm-limited conditions, were slightly faster to develop pre-feeding, and were larger post-metamorphosis; however, smaller eggs had higher fertilization when sperm was abundant, and faster planktonic development; and egg size did not affect post-metamorphic survival. The results indicate that egg size effects are conflicting in H. diramphus depending on the environments within and among life-history stages. We suggest that offspring size in this species may be a compromise between the overall costs and benefits of egg sizes in each stage and that performance in any one stage is not maximized.     

Cross‐generational effects of temperature on flight performance,and associated life‐history traits in an insect

Nongenetic parental effects may affect offspring phenotype, and in species with multiple generations per year, these effects may cause life‐history traits to vary over the season. We investigated the effects of parental, offspring developmental and offspring adult temperatures on a suite of life‐history traits in the globally invasive agricultural pest Grapholita molesta. A low parental temperature resulted in female offspring that developed faster at low developmental temperature compared with females whose parents were reared at high temperature. Furthermore, females whose parents were reared at low temperature were heavier and more fecund and had better flight abilities than females whose parents were reared at high temperature. In addition to these cross‐generational effects, females developed at low temperature had similar flight abilities at low and high ambient temperatures, whereas females developed at high temperature had poorer flight abilities at low than at high ambient temperature. Our findings demonstrate a pronounced benefit of low parental temperature on offspring performance, as well as between‐ and within‐generation effects of acclimation to low temperature. In cooler environments, the offspring generation is expected to develop more rapidly than the parental generation and to comprise more fecund and more dispersive females. By producing phenotypes that are adaptive to the conditions inducing them as well as heritable, cross‐generational plasticity can influence the evolutionary trajectory of populations. The potential for short‐term acclimation to low temperature may allow expanding insect populations to better cope with novel environments and may help to explain the spread and establishment of invasive species.     

Maternal and environmental influences on egg size and juvenile life‐history traits in Pacific salmon

Life‐history traits such as fecundity and offspring size are shaped by investment trade‐offs faced by mothers and mediated by environmental conditions. We use a 21‐year time series for three populations of wild sockeye salmon (Oncorhynchus nerka) to test predictions for such trade‐offs and responses to conditions faced by females during migration, and offspring during incubation. In years when their 1100 km upstream migration was challenged by high water discharges, females that reached spawning streams had invested less in gonads by producing smaller but not fewer eggs. These smaller eggs produced lighter juveniles, and this effect was further amplified in years when the incubation water was warm. This latter result suggests that there should be selection for larger eggs to compensate in populations that consistently experience warm incubation temperatures. A comparison among 16 populations, with matching migration and rearing environments but different incubation environments (i.e., separate spawning streams), confirmed this prediction; smaller females produced larger eggs for their size in warmer creeks. Taken together, these results reveal how maternal phenotype and environmental conditions can shape patterns of reproductive investment and consequently juvenile fitness‐related traits within and among populations.     

The offspring-development-time/offspring-number trade-off

The metabolic theory of ecology (MTE) states that metabolic rate, ruled mainly by individual mass and temperature, determines many other biological rates. This view of ecology as ruled by the laws of physics and thermodynamics contrasts with life-history-optimization (LHO) theories, where traits are shaped by evolutionary processes. Integrating the MTE and LHO can lead, however, to a synthetic theory of ecology. In this work, we link the two theories to show that offspring development time is the result of both maternal investment in offspring and the metabolic constraints on offspring growth. We formulate a model that captures how offspring development time is the consequence of both offspring growth rate, determined by temperature and allometric scaling in accordance with the MTE, and the size reached by offspring at the end of the developmental period, determined mainly by LHO and reproductive strategies. We first extend the trade-off between offspring size and offspring number to ectotherms, showing that increased body temperatures result in increased resources available for reproduction. We then combine this trade-off with the general ontogenetic growth model to show that there is a trade-off between the number of offspring produced and offspring development time. The model predicts a shorter developmental time in organisms producing larger numbers of offspring.     

Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

Population‐specific effects of developmental temperature on body condition and jumping performance of a widespread European frog

All physiological processes of ectotherms depend on environmental temperature. Thus, adaptation of physiological mechanisms to the thermal environments is important for achieving optimal performance and fitness. The European Common Frog, Rana temporaria, is widely distributed across different thermal habitats. This makes it an exceptional model for studying the adaptations to different thermal conditions. We raised tadpoles from Germany and Croatia at two constant temperature treatments (15°C, 20°C), and under natural temperature fluctuations (in outdoor treatments), and tested how different developmental temperatures affected developmental traits, that is, length of larval development, morphometrics, and body condition, as well as jumping performance of metamorphs. Our results revealed population‐specific differences in developmental time, body condition, and jumping performance. Croatian frogs developed faster in all treatments, were heavier, in better body condition, and had longer hind limbs and better jumping abilities than German metamorphs. The populations further differed in thermal sensitivity of jumping performance. While metamorphs from Croatia increased their jumping performance with higher temperatures, German metamorphs reached their performance maximum at lower temperatures. These population‐specific differences in common environments indicate local genetic adaptation, with southern populations being better adapted to higher temperatures than those from north of the Alps.     

Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages

When provisioning offspring, mothers balance the benefits of producing a few large, fitter offspring with the costs of decreased fecundity. The optimal balance between offspring size and fecundity depends on the environment. Theory predicts that larger offspring have advantages in adverse conditions, but in favorable conditions size is less important. Thus, if environmental quality varies, selection should favor mothers that adaptively allocate resources in response to local conditions to maximize maternal fitness. In the bryozoan Bugula neritina, we show that the intensity of intraspecific competition dramatically changes the offspring size/performance relationship in the field. In benign or extremely competitive environments, offspring size is less important, but at intermediate levels of competition, colonies from larger larvae have higher performance than colonies from smaller larvae. We predicted mothers should produce larger offspring when intermediate competition is likely and tested these expectations in the field by manipulating the density of brood colonies. Our findings matched expectations: mothers produced larger larvae at high densities and smaller larvae at low densities. In addition, mothers from high-density environments produced larvae that have higher dispersal potential, which may enable offspring to escape crowded environments. It appears mothers can adaptively adjust offspring size to maximize maternal fitness, altering the offspring phenotype across multiple life-history stages.     

Bet hedging in a warming ocean: predictability of maternal environment shapes offspring size variation in marine sticklebacks

Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within‐clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different‐sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within‐female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet‐hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.     

Temperature‐dependent oxygen limitation and the rise of Bergmann's rule in species with aquatic respiration

Bergmann's rule is the propensity for species‐mean body size to decrease with increasing temperature. Temperature‐dependent oxygen limitation has been hypothesized to help drive temperature–size relationships among ectotherms, including Bergmann's rule, where organisms reduce body size under warm oxygen‐limited conditions, thereby maintaining aerobic scope. Temperature‐dependent oxygen limitation should be most pronounced among aquatic ectotherms that cannot breathe aerially, as oxygen solubility in water decreases with increasing temperature. We use phylogenetically explicit analyses to show that species‐mean adult size of aquatic salamanders with branchial or cutaneous oxygen uptake becomes small in warm environments and large in cool environments, whereas body size of aquatic species with lungs (i.e., that respire aerially), as well as size of semiaquatic and terrestrial species do not decrease with temperature. We argue that oxygen limitation drives the evolution of small size in warm aquatic environments for species with aquatic respiration. More broadly, the stronger decline in size with temperature observed in aquatic versus terrestrial salamander species mirrors the relatively strong plastic declines in size observed previously among aquatic versus terrestrial invertebrates, suggesting that temperature‐dependent oxygen availability can help drive patterns of plasticity, micro‐ and macroevolution.     

Revising traditional theory on the link between plant body size and fitness under competition: evidence from old‐field vegetation

The selection consequences of competition in plants have been traditionally interpreted based on a “size‐advantage” hypothesis – that is, under intense crowding/competition from neighbors, natural selection generally favors capacity for a relatively large plant body size. However, this conflicts with abundant data, showing that resident species body size distributions are usually strongly right‐skewed at virtually all scales within vegetation. Using surveys within sample plots and a neighbor‐removal experiment, we tested: (1) whether resident species that have a larger maximum potential body size (MAX) generally have more successful local individual recruitment, and thus greater local abundance/density (as predicted by the traditional size‐advantage hypothesis); and (2) whether there is a general between‐species trade‐off relationship between MAX and capacity to produce offspring when body size is severely suppressed by crowding/competition – that is, whether resident species with a larger MAX generally also need to reach a larger minimum reproductive threshold size (MIN) before they can reproduce at all. The results showed that MIN had a positive relationship with MAX across resident species, and local density – as well as local density of just reproductive individuals – was generally greater for species with smaller MIN (and hence smaller MAX). In addition, the cleared neighborhoods of larger target species (which had relatively large MIN) generally had – in the following growing season – a lower ratio of conspecific recruitment within these neighborhoods relative to recruitment of other (i.e., smaller) species (which had generally smaller MIN). These data are consistent with an alternative hypothesis based on a ‘reproductive‐economy‐advantage’ – that is, superior fitness under competition in plants generally requires not larger potential body size, but rather superior capacity to recruit offspring that are in turn capable of producing grand‐offspring – and hence transmitting genes to future generations – despite intense and persistent (cross‐generational) crowding/competition from near neighbors. Selection for the latter is expected to favor relatively small minimum reproductive threshold size and hence – as a tradeoff – relatively small (not large) potential body size.     

Why does offspring size affect performance? Integrating metabolic scaling with life-history theory

Within species, larger offspring typically outperform smaller offspring. While the relationship between offspring size and performance is ubiquitous, the cause of this relationship remains elusive. By linking metabolic and life-history theory, we provide a general explanation for why larger offspring perform better than smaller offspring. Using high-throughput respirometry arrays, we link metabolic rate to offspring size in two species of marine bryozoan. We found that metabolism scales allometrically with offspring size in both species: while larger offspring use absolutely more energy than smaller offspring, larger offspring use proportionally less of their maternally derived energy throughout the dependent, non-feeding phase. The increased metabolic efficiency of larger offspring while dependent on maternal investment may explain offspring size effects—larger offspring reach nutritional independence (feed for themselves) with a higher proportion of energy relative to structure than smaller offspring. These findings offer a potentially universal explanation for why larger offspring tend to perform better than smaller offspring but studies on other taxa are needed.     

Temperature‐size relations from the cellular‐genomic perspective

A family of empirically based ecological ‘rules’, collectively known as temperature‐size rules, predicts larger body size in colder environments. This prediction is based on studies demonstrating that a wide range of ectotherms show increased body size, cell size or genome size in low‐temperature habitats, or that individuals raised at low temperature become larger than conspecifics raised at higher temperature. There is thus a potential for reduction in size with global warming, affecting all levels from cell volume to body size, community composition and food webs. Increased body size may be obtained either by increasing the size or number of cells. Processes leading to changed cell size are of great interest from an ecological, physiological and evolutionary perspective. Cell size scales with fundamental properties such as genome size, growth rate, protein synthesis rates and metabolic activity, although the causal directions of these correlations are not clear. Changes in genome size will thus, in many cases, not only affect cell or body size, but also life‐cycle strategies. Symmetrically, evolutionary drivers of life‐history strategies may impact growth rate and thus cell size, genome size and metabolic rates. Although this goes to the core of many ecological processes, it is hard to move from correlations to causations. To the extent that temperature‐driven changes in genome size result in significant differences among populations in body size, allometry or life‐cycle events such as mating season, it could serve as a fast route to speciation. We offer here a novel perspective on the temperature‐size rules from a ‘bottom‐up’ perspective: how temperature may induce changes in genome size, and thus implicitly in cell size and body size of metazoans. Alternatively: how temperature‐driven enlargement of cells also dictates genome‐size expansion to maintain the genome‐size to cell‐volume ratio. We then discuss the different evolutionary drivers in aquatic versus terrestrial systems, and whether it is possible to arrive at a unifying theory that also may serve as a predictive tool related to temperature changes. This, we believe, will offer an updated review of a basic concept in ecology, and novel perspectives on the basic biological responses to temperature changes from a genomic perspective.     

SIZE‐FECUNDITY RELATIONSHIPS,GROWTH TRAJECTORIES,AND THE TEMPERATURE‐SIZE RULE FOR ECTOTHERMS

Many ectotherms show crossing growth trajectories as a plastic response to rearing temperature. As a result, individuals growing up in cool conditions grow slower, mature later, but are larger at maturation than those growing up in warm conditions. To date, no entirely satisfactory explanation has been found for why this pattern, often called the temperature‐size rule, should exist. Previous theoretical models have assumed that size‐specific mortality rates were most likely to drive the pattern. Here, I extend one theoretical model to show that variation in size‐fecundity relationships may also be important. Plasticity in the size‐fecundity relationship has rarely been considered, but a number of studies show that fecundity increases more quickly with size in cold environments than it does in warm environments. The greater increase in fecundity offsets costs of delayed maturation in cold environments, favoring a larger size at maturation. This can explain many cases of crossing growth trajectories, not just in relation to temperature.     

Energetic cost of calling: general constraints and species‐specific differences

The energetic cost of acoustic signalling varies tremendously among species. Understanding factors responsible for this heterogeneity is important for understanding the costs and benefits of signalling. Here, we present a general model, based on well‐established principles of bioenergetics, which predicts the energetic cost of call production across species. We test model predictions using an extensive database of resting and calling metabolic rates of insects, amphibians and birds. Results are largely supportive of model predictions. Calling metabolic rates scale predictably with body mass and temperature such that calling and resting metabolic rates are directly proportional to each other. The cost of acoustic signalling is ～8 times higher than resting metabolic rate in ectotherms, and ～2 times higher in birds. Differences in the increase in metabolic rate during calling are explained by the relative size of species’ sound‐producing muscles. Combined with published work, we quantify call efficiency and discuss model implications.     

Maternal effects across life stages: larvae experiencing predation risk increase offspring provisioning

1. Maternal provisioning can reduce offspring vulnerability to predators by promoting offspring growth and eliciting of antipredator behaviours. Mothers perceiving predation risk may improve offspring survival if producing larger, higher‐quality offspring. However, empirical evidence suggests that offspring quality is often reduced, probably reflecting predator‐induced physiological costs, or a selfish maternal strategy aimed at producing more offspring by sacrificing their quality. While perception and impact of predators can vary across the prey's life stage, a majority of studies have focused on understanding how reproductive allocation decisions are influenced by the risk of predation during adulthood. 2. In this study, Leptinotarsa decemlineata beetles were used to examine if the risk of predation during the larval stage: (i) impacts the mother's physiological condition, including body mass and metabolic rate; and (ii) alters maternal allocation of reproductive resources to offspring quantity versus quality. 3. Results revealed that L. decemlineata mothers responded to perceived predation risk by producing clutches with fewer but larger eggs, thus increasing offspring provisioning. Surprisingly, while females that had faced predation risk as larva emerged with a similar body mass to control females, they exhibited lower metabolic rates. 4. Although predation risk in L. decemlineata larvae is known to impair their ability to acquire and maintain energy resources, adult females appeared to ameliorate such costs by improving their metabolic efficiency and by allocating more of their limited reproductive resources to produce fewer but better‐quality offspring.     

Urbanization disrupts latitude‐size rule in 17‐year cicadas

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.     

Transgenerational developmental effects of species‐specific,maternally transmitted microbiota in Onthophagus dung beetles

1. The significance of host–microbe interactions is increasingly appreciated across biological disciplines, yet to what extent these interactions influence developmental outcomes within and across generations remains poorly understood. 2. This study investigated the putative role of host–microbe interactions in the adaptive diversification of Onthophagus dung beetles, one of the most species‐rich and ecologically successful genera of insects. Onthophagus mothers vertically transmit growth‐ and fitness‐enhancing gut symbionts to their offspring through a faecal secretion known as the pedestal. 3. Pedestals were reciprocally exchanged between two ecologically similar congeneric Onthophagus species to assess the degree to which pedestal microbiota from one species can substitute for those of another. 4. It was found that the presence of a heterospecific pedestal delays development and increases mortality, and that the fitness costs of non‐host‐specific microbiota are maintained transgenerationally. 5. Collectively, these results support the hypothesis that Onthophagus beetles maintain, interact with, and are dependent upon host species‐specific microbial communities to support normal growth and development. The implications of these results are discussed in the context of host microbiota coevolution.     

Lesser double‐collared sunbirds Nectarinia chalybea do not compensate for hatching asynchrony by adjusting egg mass or yolk androgens

Substantial amounts of maternal androgens are found in birds’ eggs and have been shown to benefit offspring development. Within‐clutch patterns of increasing androgen concentrations over the laying sequence are often hypothesized to compensate for the negative effects of hatching asynchrony. However, detrimental effects to offspring fitness of exposure to high yolk androgen levels have also been demonstrated. This suggests that mothers should forego these costs to their offspring when the need for compensation for hatching asynchrony is low or when alternative compensatory strategies, e.g. in terms of increasing egg mass, are available. Here we show that in the south‐temperate lesser double‐collared sunbird Nectarinia chalybea, a species with hatching asynchrony but also with high survival of last‐hatched chicks, mothers do not deposit resources differentially in terms of either yolk androgen concentration or egg mass across the laying sequence. We discuss to what extend this challenges the original explanation of within‐clutch variation in these egg parameters and offer some explanation for their between‐clutch variation which was related to female body mass.     

The impacts of extreme and fluctuating temperatures on trait‐mediated indirect aphid–parasitoid interactions

1. Global climate change models predict an increase in the frequency and magnitude of extreme temperature events. These temperature events, heatwaves for example, will impact a wide range of physiological and behavioural processes, particularly in ectotherms, and may therefore influence interactions between species. 2. Anti‐predator responses may be more costly under more severe temperature regimes and therefore trait‐mediated disturbance could lead to high mortality or reduced reproduction under extreme and fluctuating temperature regimes. 3. We examined the impacts of extreme and fluctuating temperatures on trait‐mediated indirect interactions in an aphid–parasitoid community. 4. In treatments that isolated the effects of trait‐mediated disturbance from the effects of foraging parasitoids we found that an increase in both the amplitude and frequency of peak temperatures reduced aphid numbers and provided evidence that the cost of trait‐mediated disturbance could increase under frequent periods of high temperature. Aphid dispersal also increased with more frequent periods of high temperature. 5. In treatments where female wasps were allowed to freely forage (direct + trait‐mediated effects), there was no evidence that extreme and fluctuating temperatures influenced the wasp's foraging ability. Exposure to extreme fluctuating temperatures did not influence the offspring production of exposed wasps or the position of the mummies within the plots.     

COSTLY INFIDELITY: LOW LIFETIME FITNESS OF EXTRA‐PAIR OFFSPRING IN A PASSERINE BIRD

Extra‐pair copulation (EPC) is widespread in socially monogamous species, but its evolutionary benefits remain controversial. Indirect genetic benefit hypotheses postulate that females engage in EPC to produce higher quality extra‐pair offspring (EPO) than within‐pair offspring (WPO). In contrast, the sexual conflict hypothesis posits that EPC is beneficial to males but not to females. Thus, under the sexual conflict hypothesis, EPO are predicted to be no fitter than WPO. We tested these two hypotheses in a 12‐year dataset with complete life‐history and pedigree information from an isolated island population of house sparrows (Passer domesticus). We compared fitness components of EPO and two types of WPO: (1) WPO from genetically polyandrous “unfaithful” mothers, and (2) WPO from genetically monogamous mothers. We found that all three groups of offspring had similar probabilities of hatching and nestling survival. Unexpectedly, EPO had the lowest probability of recruiting into the breeding population and the lowest lifetime reproductive output. Our results indicate that EPO incurred indirect genetic costs, rather than benefits, which is contrary to indirect benefit models. Importantly, the indirect costs we observed are also underappreciated in current sexual conflict models. Our results call for improved theoretical frameworks that incorporate indirect costs by extending current sexual conflict models.