Yolanda E. Morbey

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.

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 hypotheses for protandry in arrival to breeding areas: a review of models and empirical tests

Our understanding of avian migration has progressed significantly, yet the selective conditions that favor the arrival of males before females at the site of reproduction remain largely unclear. Here, we review the leading adaptive hypotheses for protandry, highlight some key empirical studies that test protandry theory, and identify theoretical and empirical information demands. In general, protandry should evolve in species where the variance in male reproductive success is larger than in females if the costs to males of earlier arrival relative to calendar date (viability selection) can be balanced by increased mating opportunities (sexual selection). Early arrival by males can provide ‘priority benefits’ that help in the monopolization of resources or ‘early bird draw benefits’ that increase opportunities for extra-pair mating. While some empirical studies are consistent with theoretical predictions regarding the important selection factors that influence protandry (e.g., extrinsic mortality and extra-pair paternity), some are not, and some studies focus on ecological factors that have not been considered explicitly by theory. We call for an integrated theoretical approach to help formalize how protandry should evolve in response to the antagonistic roles of natural and sexual selection, the nature of competitive asymmetries among males or females, sex-specific costs and benefits of early arrival, and various climate change scenarios.

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.

Intraspecific Variability in Nestling Growth and Fledging Behavior of Cassin's Auklets at Triangle Island, British Columbia

We compared nestling growth and fledging behavior of Cassins Auklets (Ptychoramphus aleuticus) at Triangle Island, British Columbia to the predictions of a model that considers the timing of fledging to be an adaptive strategy. In the model, fledging mass and age depend on nestling growth rate, time remaining in the season, and the contrasting mortality costs and growth benefits experienced before and after fledging. As predicted, fast growing nestlings fledged heavier and younger than slow growing nestlings. Growth rates declined over the season and fledging behavior varied accordingly. When the seasonal variation in growth rates was statistically controlled, late nestlings did not fledge lighter and younger, in contrast to the models predictions. Late in the season, nestlings reached a greater peak mass than expected based on their slower growth rates. Also, nestlings that grew more slowly due to a higher frequency of handling reached a higher peak mass than less frequently measured nestlings. We consider the possibility that parents adaptively modified their nestlings growth trajectory by altering provisioning behavior in response to nestling condition. The nesting habitat influenced fledging. Fast growing nestlings fledged at similar ages in both level and steep nest sites. In contrast, slow growing nestlings fledged at younger ages, but similar masses, in level sites compared to steep sites. We consider the possibility that the difference in parental predation risk between level and steep nest sites influenced provisioning decisions of parents, and consequently, fledging decisions of nestlings.

The interaction between reproductive lifespan and protandry in seasonal breeders.

The timing and duration of reproductive activities are highly variable both at the individual and population level. Understanding how this variation evolved by natural selection is fundamental to understanding many important aspects of an organisms life history, ecology and behaviour. Here, we combine game theoretic principles governing reproductive timing and the evolutionary theory of senescence to study the interaction between protandry (the earlier arrival or emergence of males to breeding areas than females) and senescence in seasonal breeders. Our general model applies to males who are seeking to mate as frequently as possible over a relatively short period, and so is relevant to many organisms including annual insects and semelparous vertebrates. The model predicts that protandry and maximum reproductive lifespans should increase in environments characterized by high survival and by a low competitive cost of maintaining the somatic machinery necessary for survival. In relatively short seasons under these same conditions, seasonal declines in the reproductive lifespans of males of equivalent quality will be evolutionarily stable. However, over a broad range of potential values for daily survival and maintenance cost, reproductive lifespan is expected to be relatively short and constant throughout a large fraction of the season. We applied the model to sockeye (or kokanee) salmon Oncorhynchus nerka and show that pronounced seasonal declines in reproductive lifespan, a distinctive feature of semelparous Oncorhynchus spp., is likely part of a male mating strategy to maximize mating opportunities.

Pair formation, pre-spawning waiting, and protandry in kokanee, Oncorhynchus nerka

The timing of arrival to breeding areas can have profound effects on reproductive success. Under some conditions (restricted breeding seasons and mating systems characterized by a longer period of mating among males than females), the maximization of mating opportunities by males theoretically selects for the earlier arrival of males than females (a phenomenon called protandry). This study quantifies the relationship between the arrival timing and spawning success of male kokanee (non-anadromous Oncorhynchus nerka). The spawning behavior of kokanee was observed in a large pen and the spawning success of each male was estimated as the number of spawning events he participated in. A males spawning success depended primarily on his success at pairing with and mate-guarding females, and less on participation in spawning events while unpaired. Males who paired earlier in the season had higher spawning success than males who paired later in the season because they experienced more opportunities to pair with new females. Among males who eventually paired (some males never did), arriving early was correlated with pairing early. However, selection for protandry was weak, largely because early arrival did not guarantee that a male would pair. Pre-spawning waiting by females also weakened the correlation between arrival day and pairing day. The random probability of pairing with respect to arrival day and pre-spawning waiting by females likely explains the weak selection for protandry in kokanee and the low amount of protandry observed in other sockeye salmon (anadromous O. nerka) populations.

Dynamics of Piscivory by Lake Trout following a Smallmouth Bass Invasion: A Historical Reconstruction

Our objective was to assess the dynamics of piscivory by lake trout Salvelinus namaycush in Lake Opeongo, Ontario, following the introduction of smallmouth bass Micropterus dolomieu early in the 1900s. The effects of this introduction on lake trout were thought to be of slight significance at the time, but they may have been obscured by the introduction of cisco Coregonus artedi in 1948. Our analyses of lake trout stomach contents and stable isotopes of archived scales indicated that several dietary changes occurred in advance of the cisco introduction. These changes included the consumption of fewer yellow perch Perca flavescens, fewer but larger lake whitefish C. clupeaformis, and larger lake whitefish for a given lake trout size. Stable isotope analyses were consistent with a decline in the importance of littoral prey for young lake trout before the introduction of cisco. We hypothesize that the indirect effects of smallmouth bass on the pelagic fish community explain these patterns.

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.

Intermittent breeding in the absence of a large cost of reproduction: evidence for a non‐migratory, iteroparous salmonid

In long-lived organisms, intermittent breeding likely evolves as a resource allocation strategy for coping with environmental uncertainty or individual heterogeneity in condition. In fishes, the phenomenon of intermittent breeding is referred to as skipped spawning, and appears to be more common at high latitudes or in migratory species with high accessory costs of reproduction. We used long-term monitoring data on lake trout (Salvelinus namaycush) to test whether key predictions about the frequency of skipped spawning hold in a mid-latitude population of a species lacking any obvious costs of reproduction beyond the production and fertilization of gametes. We first developed a threshold-based method to classify skipped spawners based on gonad size, fish size, and fish age. Consistent with life history theory, age-specific frequencies of skipped spawning were higher in females than males. The frequency of skipped spawning varied among years and was higher in 1994–2011 than in 1938–1959, perhaps because of food web changes over the past century. In temperate lakes, food web structure may be sufficiently variable to favor intermittent breeding in long-lived iteroparous fishes, despite low accessory costs of reproduction.