Juvenile-to-adult transition invariances in fishes: Perspectives on proximate and ultimate causation.

To bridge physiological and evolutionary perspectives on size at maturity in fishes, the authors focus on the approximately invariant ratio between the estimated oxygen supply at size at maturity (Qm ) relative to that at asymptotic size (Q∞ ) among species within a taxonomic group, and show how two important theories related to this phenomenon complement each other. Gill-oxygen limitation theory proposes a mechanistic basis for a universal oxygen supply-based threshold for maturation, which applies among and within species. On the contrary, the authors show that a generalisation of life-history theory for the invariance of size at maturity (Lm ) relative to asymptotic size (L∞ ) can provide an evolutionary rationale for an oxygen-limited maturation threshold (Qm /Q∞ ). Extending previous inter- and intraspecific analyses, the authors show that maturation invariances also occur in lake whitefish Coregonus clupeaformis (Mitchill 1818), but at both scales, theory seems to underestimate the value of the maturation threshold. They highlight some key uncertainties in the model that should be addressed to help resolve the mismatch.

Experimental ghrelin administration affects migratory behaviour in a songbird.

Twice a year, billions of birds take on drastic physiological and behavioural changes to migrate between breeding and wintering areas. On migration, most passerine birds regularly stop over along the way to rest and refuel. Endogenous energy stores are not only the indispensable fuel to complete long distance flights, but are also important peripheral signals that once integrated in the brain modulate crucial behavioural decisions, such as the decision to resume migration after a stopover. A network of hormones signals metabolic fuel availability to the brain in vertebrates, including the recently discovered gut-hormone ghrelin. Here, we show that ghrelin takes part in the control of migratory behaviour during spring migration in a wild migratory passerine. We manipulated blood concentrations of ghrelin of 53 yellow-rumped warblers (Setophaga coronata coronata) caught during stopover and automatically radio-tracked their migratory behaviour following release. We found that injections of acylated and unacylated ghrelin rapidly induced movements away from the release site, indicating that the ghrelin system acts centrally to mediate stopover departure decisions. The effects of the hormone manipulation declined within 8 h following release, and did not affect the overall rate of migration. These results provide experimental evidence for a pivotal role of ghrelin in the modulation of behavioural decisions during migration. In addition, this study offers insights into the regulatory functions of metabolic hormones in the dialogue between gut and brain in birds.

Using breath δ13C analysis to determine the effects of dietary carbohydrate and protein on glucose and leucine oxidation at rest in the yellow-rumped warbler (Setophaga coronata).

Fat is the major fuel for migratory flight of birds, but protein is also catabolized. Flight range could be reduced if protein is used too quickly from muscles and organs, and it is important to understand factors that influence protein catabolism. Previous correlative studies suggested high protein diets may increase protein use in flight, although a wind tunnel study with yellow-rumped warblers (Setophaga coronata) did not support this relationship. We tested the hypothesis that diet composition affects nutrient oxidation in resting, fasted yellow-rumped warblers. For method development, we gavaged or subcutaneously injected warblers with 13C labelled glucose or leucine, and measured δ13C of breath CO2 in real time using infrared laser spectrometry. Regardless of route of administration, leucine had greater instantaneous and cumulative oxidation than glucose. Compared to subcutaneous injection, gavaged birds reached maximum oxidation rate faster for leucine and glucose, respectively, had a higher maximum oxidation rate, and reached final cumulative oxidation approximately faster for leucine or glucose, respectively, indicating immediate oxidation of the substrates by the digestive system. Warblers (N = 10 each) were fed isocaloric 60% carbohydrate or 60% protein diets for minimum 2 weeks, and subcutaneously injected with 13C labelled glucose or leucine. Diet composition had little effect on oxidation kinetics except that warblers fed high-carbohydrate reached final cumulative oxidation of leucine more quickly than those fed high-protein. The findings do not support the hypothesis that high protein diets increase the oxidation of protein during negative energy states in migratory birds, and provide methodology that could be applied to test it in flight.

Reproductive consequences of an extra long-term sperm storage organ.

BACKGROUND: Sperm storage plays a key role in the reproductive success of many sexually-reproducing organisms, and the capacity of long-term sperm storage varies across species. While there are theoretical explanations for why such variation exists, to date there are no controlled empirical tests of the reproductive consequences of additional long-term sperm storage. While Dipterans ancestrally have three long-term sperm organs, known as the spermathecae, Drosophila contain only two. RESULTS: We identified a candidate gene, which we call spermathreecae (sp3), in which a disruption cause the development of three functional spermathecae rather than the usual two in Drosophila. We used this disruption to test the reproductive consequences of having an additional long-term sperm storage organ. Compared to females with two spermathecae, females with three spermathecae store a greater total number of sperm and can produce offspring a greater length of time. However, they did not produce a greater total number of offspring. CONCLUSIONS: Thus, additional long-term sperm storage in insects may increase female fitness through extending the range of conditions where she produces offspring, or through increasing the quality of offspring via enhanced local sperm competition at fertilization.

Elevated incubation temperature improves later-life swimming endurance in juvenile Chinook salmon, Oncorhynchus tshawytscha.

The effect of incubation and rearing temperature on muscle development and swimming endurance under a high-intensity swimming test was investigated in juvenile Chinook salmon (Oncorhynchus tshawytscha) in a hatchery experiment. After controlling for the effects of fork length (LF ) and parental identity, times to fatigue of fish were higher when fish were incubated or reared at warmer temperatures. Significant differences among combinations of pre- and post-emergence temperatures conformed to 15-15°C > 15-9°C > 9-9°C > 7-9°C > 7-7°C in 2011 when swimming tests were conducted at 300 accumulated temperature units post-emergence and 15-9°C > (7-9°C = 7-7°C) in 2012 when swimming tests were conducted at an LF of c. 40 mm. The combination of pre- and post-emergence temperatures also affected the number and size of muscle fibres, with differences among temperature treatments in mean fibre cross-sectional area persisting after controlling for LF and parental effects. Nonetheless, neither fibre number nor fibre size accounted for significant variation in swimming endurance. Thus, thermal carryover effects on swimming endurance were not mediated by thermal imprinting of muscle structure. This is the first study to test how temperature, body size and muscle structure interact to affect swimming endurance during early development in salmon.

Stopover refuelling, movement and departure decisions in the white-throated sparrow: The influence of intrinsic and extrinsic factors during spring migration.

Differential migration timing between sex or age classes is an example of how migratory movement strategies can differ among subgroups within a population. However, in songbirds, evidence for intrinsic differences in en route migratory behaviour is often mixed, suggesting that the local environmental context may play a role in accentuating or diminishing patterns. We evaluated how multiple intrinsic and extrinsic variables influenced refuelling rates, local movement behaviour and departure decisions in the white-throated sparrow Zonotrichia albicollis during spring migration. This species exhibits a unique genetically based plumage dimorphism, providing a unique class of individual in which to evaluate patterns and processes of differential migration, in addition to sex, age and migration distance. At a migratory stopover site, plasma metabolite analysis was used to quantify individual variation in stopover refuelling rate. In after second year adults, automated and manual radio telemetry was used to quantify daily activity timing, daily movement distances, stopover duration and departure time. Arrival timing to the stopover site was determined using capture data. Non-breeding and previous breeding/natal latitude were determined using analysis of hydrogen isotopes in claws and feathers. Males arrived at the stopover site 11 days on average before females, but no difference in migration timing was observed between plumage morph or age classes. After second year, adults with more southern previous breeding latitudes arrived at stopover earlier, whereas second year birds making their first return migration arrived at stopover in an inverse relationship to non-breeding latitude. Stopover refuelling rate did not differ between ages, sexes or plumage morphs, and daily departure probability of adults was higher under warmer temperatures and favourable tailwinds. White-striped morphs moved greater distances during stopover, initiated daily activity earlier in the morning and departed for migration earlier in the evening than tan-striped morphs. Our results show that while individual phenotype can influence some aspects of local stopover-scale movement behaviour, evidence for differential stopover behaviour was weak. Differential migration timing is unlikely to result from intrinsic differences in en route refuelling rate and departure decisions, especially because the latter is strongly influenced by meteorological conditions.

Size-selective fishing and the potential for fisheries-induced evolution in lake whitefish.

The long-term evolutionary effects of fishing on maturation schedules can depend on gear type, the shape of the gear type's size-selectivity function, and the size and age structure of a population. Our goal was to better understand how environmentally induced differences in somatic growth influence the evolutionary effects of size-selective fisheries, using lake whitefish (Coregonus clupeaformis) in Lake Huron as a case study. Using a state-dependent optimization model of energy allocation parameterized for lake whitefish, we show that fishing with gill nets (bell-shaped selectivity) and trap nets (sigmoid-shaped selectivity) can be potent agents of selection on size thresholds for maturity. Compared to trap nets and large mesh (114 mm) gill nets, small mesh (89 mm) gill nets are better able to buffer populations from fishing-induced evolution by safeguarding large, fecund fish, but only when overall fishing mortality is low and growth rates sufficiently fast such that fish can outgrow vulnerable size classes. Regardless of gear type, and all else being equal, high fishing mortality in combination with low growth rates is expected to intensify the long-term evolutionary effects of fishing.

Female-biased dimorphism in size and age at maturity is reduced at higher latitudes in lake whitefish Coregonus clupeaformis.

Female-biased sexual dimorphism in size at maturity is a common pattern observed in freshwater fishes with indeterminate growth, yet can vary in magnitude among populations for reasons that are not well understood. According to sex-specific optimization models, female-biased sexual size dimorphism can evolve due to sexual selection favouring earlier maturation by males, even when sexes are otherwise similar in their growth and mortality regimes. The magnitude of sexual size dimorphism is expected to depend on mortality rate. When mortality rates are low, both males and females are expected to mature at older ages and larger sizes, with size determined by the von Bertalanffy growth equation. The difference between size at maturity in males and females becomes reduced when maturing at older ages, closer to asymptotic size. This phenomenon is called von Bertalanffy buffering. The predicted relationship between the magnitude of female-biased sexual dimorphism in age and size at maturity and mortality rate was tested in a comparative analysis of lake whitefish Coregonus clupeaformis from 26 populations across a broad latitudinal range in North America. Most C. clupeaformis populations displayed female-biased sexual dimorphism in size and age at 50% maturity. As predicted, female-biased sexual size dimorphism was less extreme among lower mortality, high-latitude populations.

Egg size and the adaptive capacity of early life history traits in Chinook salmon (Oncorhynchus tshawytscha).

Offspring traits are greatly influenced by maternal effects, and these maternal effects may provide an important pathway through which populations can adapt to changing thermal environments. We investigated the effect of egg size on the among- and within-population variation in early life history traits among introduced Great Lakes Chinook salmon (Oncorhynchus tshawytscha) populations under varying thermal conditions. We reared Chinook salmon from three populations in a common-garden hatchery study at 6.5, 9.4, and 15.2°C and measured a variety of fitness-related traits during development. We found that most of the among-population variation in early life history traits was explained by egg size. However, the contribution of egg size to the among-population variation decreased with an increase in temperature suggesting that other effects, such as genetic, contribute at high temperature. Within populations, egg size explained much of the dam variance and maternal effect for traits in every temperature, whereas egg size generally had little to no influence on the sire variance and heritability. Overall, our results demonstrate the significant contribution egg size makes to shaping early life history phenotypes among and within populations, and suggest that egg size is an important pathway through which offspring phenotypes can evolve on contemporary timescales.

Adcyap1 polymorphism covaries with breeding latitude in a Nearctic migratory songbird, the Wilson's warbler (Cardellina pusilla).

Understanding the genetic background of complex behavioral traits, showing multigenic control and extensive environmental effects, is a challenging task. Among such traits, migration is known to show a large additive genetic component. Yet, the identification of specific genes or gene regions explaining phenotypic variance in migratory behavior has received less attention. Migration ultimately depends on seasonal cycles, and polymorphism at phenological candidate genes may underlie variation in timing of migration or other aspects of migratory behavior. In this study of a Nearctic-Neotropical migratory songbird, the Wilson's warbler (Cardellina pusilla), we investigated the association between polymorphism at two phenological candidate genes, Clock and Adcyap1, and two aspects of the migratory phenotype, timing of spring migration through a stopover site and inferred latitude of the breeding destination. The breeding destination of migrating individuals was identified using feather deuterium ratio (δ (2)H), which reliably reflects breeding latitude throughout the species' western breeding range. Ninety-eight percent of the individuals were homozygous at Clock, and the rare heterozygotes did not deviate from homozygous migration phenology. Adcyap1 was highly polymorphic, and allele size was not significantly associated with migration date. However, Adcyap1 allele size significantly positively predicted the inferred breeding latitude of males but not of females. Moreover, we found a strong positive association between inferred breeding latitude and Adcyap1 allele size in long-distance migrating birds from the northern sector of the breeding range (western Canada), while this was not the case in short-distance migrating birds from the southern sector of the breeding range (coastal California). Our findings support previous evidence for a role of Adcyap1 in shaping the avian migratory phenotype, while highlighting that patterns of phenological candidate gene-phenotype associations may be complex, significantly varying between geographically distinct populations and even between the sexes.

Time scale matters: genetic analysis does not support adaptation-by-time as the mechanism for adaptive seasonal declines in kokanee reproductive life span.

Seasonal declines of fitness-related traits are often attributed to environmental effects or individual-level decisions about reproductive timing and effort, but genetic variation may also play a role. In populations of Pacific salmon (Oncorhynchus spp.), seasonal declines in reproductive life span have been attributed to adaptation-by-time, in which divergent selection for different traits occurs among reproductively isolated temporal components of a population. We evaluated this hypothesis in kokanee (freshwater obligate Oncorhynchus nerka) by testing for temporal genetic structure in neutral and circadian-linked loci. We detected no genetic differences in presumably neutral loci among kokanee with different arrival and maturation dates within a spawning season. Similarly, we detected no temporal genetic structure in OtsClock1b, Omy1009uw, or OmyFbxw11, candidate loci associated with circadian function. The genetic evidence from this study and others indicates a lack of support for adaptation-by-time as an important evolutionary mechanism underlying seasonal declines in reproductive life span and a need for greater consideration of other mechanisms such as time-dependent, adaptive adjustment of reproductive effort.

A genetic test of sexual size dimorphism in pre-emergent chinook salmon.

Sex differences in early development may play an important role in the expression of sexual size dimorphism at the adult stage. To test whether sexual size dimorphism is present in pre-emergent chinook salmon (Oncorhynchus tshawytscha), alevins were reared at two temperatures (10 °C and 15 °C) and sexed using the OtY1 marker on the Y-chromosome. Linear mixed models were used to test for sex differences in alevin size within families while controlling for the random effects of sire and dam nested within sire. Males and females did not differ in weight at 10 °C but males were heavier than females at 15 °C. Sex accounted for 2% of the within-family variance in weight. In addition, at 15°C, the relationship between weight and sex was greater in families with larger eggs. Whereas male-biased sexual size dimorphism was present at the juvenile stage, female-biased sexual size dimorphism was present at sexual maturity. Males were also younger than females at sexual maturity. A head start on growth by males may underlie their earlier maturation at a smaller size, thus leading to female-biased SSD at the adult stage.

Protandry, sexual size dimorphism, and adaptive growth.

Adaptive growth refers to the strategic adjustment of growth rate by individuals to maximize some component of fitness. The concept of adaptive growth proliferated in the 1990s, in part due to an influential theoretical paper by Peter Abrams and colleagues. In their 1996 paper, Abrams et al. explored the effects of time stress on optimal growth rate, development time, and adult size in seasonal organisms. In this review, I explore how the concept of adaptive growth informs our understanding of protandry (the earlier arrival of males to sites of reproduction than females) and sexual size dimorphism in seasonal organisms. I conclude that growth rate variation is an important mechanism that helps to conserve optimal levels of protandry and sexual size dimorphism in changing environments.

Rapid senescence in pacific salmon.

Any useful evolutionary theory of senescence must be able to explain variation within and among natural populations and species. This requires a careful characterization of age-specific mortality rates in nature as well as the intrinsic and extrinsic factors that influence these rates. We perform this task for two populations of semelparous Pacific salmon. During the breeding season, estimated daily mortality rates increased from 0 to 0.2-0.5 (depending on the year) over the course of several weeks. Early-arriving individuals had a later onset and/or a lower rate of senescence in each breeding season, consistent with adaptive expectations based on temporal variation in selection. Interannual variation in senescence was large, in part because of extrinsic factors (e.g., water temperature). Predation rates were higher in Pick Creek sockeye salmon (anadromous Oncorhynchus nerka) than in Meadow Creek kokanee (nonanadromous O. nerka), but in contrast to evolutionary theory, senescence was not more rapid in the former. Interannual variation may have obscured interpopulation divergence in senescence. Pacific salmon are a promising system for further studies on the physiological, evolutionary, and genetic bases of senescence. In particular, we encourage further research to disentangle the relative importance of adaptive and nonadaptive variation in senescence.

Adaptive variation in senescence: reproductive lifespan in a wild salmon population.

The antagonistic pleiotropy theory of senescence postulates genes or traits that have opposite effects on early-life and late-life performances. Because selection is generally weaker late in life, genes or traits that improve early-life performance but impair late-life performance should come to predominate. Variation in the strength of age-specific selection should then generate adaptive variation in senescence. We demonstrate this mechanism by comparing early and late breeders within a population of semelparous capital-breeding sockeye salmon (Oncorhynchus nerka). We show that early breeders (but not late breeders) are under strong selection for a long reproductive lifespan (RLS), which facilitates defence of their nests against disturbance by later females. Accordingly, early females invest less energy in egg production while reserving more for nest defence. Variation along this reproductive trade-off causes delayed or slower senescence in early females (average RLS of 26 days) than in late females (reproductive lifespan of 12 days). We use microsatellites to confirm that gene flow is sufficiently limited between early and late breeders to allow adaptive divergence in response to selection. Because reproductive trade-offs should be almost universal and selection acting on them should typically vary in time and space, the mechanism described herein may explain much of the natural variation in senescence.

Timing games in the reproductive phenology of female pacific salmon (Oncorhynchus spp.).

We use a game-theoretic framework to investigate the reproductive phenology of female kokanee (Oncorhynchus nerka). As in the other semelparous species of Pacific salmon, females construct nests in gravel, spawn with males, bury their fertilized eggs, and defend their nest sites until they die several days later. Later-breeding females may reuse previous nest sites, and their digging behavior is thought to subject previously buried eggs to mortality. Using game-theoretic models, we show that females can reduce this risk by allocating resources to longevity (the period between arrival and death) as opposed to eggs. Waiting before territory settlement is also expected if it allows females to conserve energy and delay senescence. The models demonstrate how these costs and benefits interact to select for a seasonal decline in longevity, a well-known phenomenon in the salmonid literature, and a seasonal decline in wait duration. Both of these predictions were supported in a field study of kokanee. Female state of reproductive maturity was the most important proximate factor causing variation in longevity and wait duration. With more than 30% of territories being reused, dig-up is likely an important selective force in this population.