Thomas E. Reed

Phenotypic plasticity and population viability: the importance of environmental predictability

Phenotypic plasticity plays a key role in modulating how environmental variation influences population dynamics, but we have only rudimentary understanding of how plasticity interacts with the magnitude and predictability of environmental variation to affect population dynamics and persistence. We developed a stochastic individual-based model, in which phenotypes could respond to a temporally fluctuating environmental cue and fitness depended on the match between the phenotype and a randomly fluctuating trait optimum, to assess the absolute fitness and population dynamic consequences of plasticity under different levels of environmental stochasticity and cue reliability. When cue and optimum were tightly correlated, plasticity buffered absolute fitness from environmental variability, and population size remained high and relatively invariant. In contrast, when this correlation weakened and environmental variability was high, strong plasticity reduced population size, and populations with excessively strong plasticity had substantially greater extinction probability. Given that environments might become more variable and unpredictable in the future owing to anthropogenic influences, reaction norms that evolved under historic selective regimes could imperil populations in novel or changing environmental contexts. We suggest that demographic models (e.g. population viability analyses) would benefit from a more explicit consideration of how phenotypic plasticity influences population responses to environmental change.

Reproductive Senescence in a Long‐Lived Seabird: Rates of Decline in Late‐Life Performance Are Associated with Varying Costs of Early Reproduction

Evolutionary theories of senescence predict that rates of decline in performance parameters should be shaped by early‐life trade‐offs between reproduction and somatic maintenance. Here we investigate factors influencing the rate of reproductive senescence in a long‐lived seabird, the common guillemot Uria aalge, using data collected over a 23‐year period. In the last 3 years of life, individual guillemots had significantly reduced breeding success and were less likely to hold a site or attempt to breed. Females senesced at a significantly faster rate than males. At the individual level, high levels of reproductive output earlier in life were associated with increased senescence later in life. This trade‐off between early‐ and late‐life reproduction was evident independent of the fact that as birds age, they breed later in the season. The rate of senescence was additionally dependent on environmental conditions experienced earlier in life, with evidence that harsh conditions amplified later declines in breeding success. Overall, individuals with intermediate levels of early‐life productivity lived longer. These results provide support for the antagonistic‐pleiotropy and disposable‐soma theories of senescence and demonstrate for the first time in a wild bird population that increased rates of senescence in reproductive performance are associated with varying costs of reproduction early in life.

Interacting Effects of Phenotypic Plasticity and Evolution on Population Persistence in a Changing Climate

Abstract Climate change affects individual organisms by altering development, physiology, behavior, and fitness, and populations by altering genetic and phenotypic composition, vital rates, and dynamics. We sought to clarify how selection, phenotypic plasticity, and demography are linked in the context of climate change. On the basis of theory and results of recent empirical studies of plants and animals, we believe the ecological and evolutionary issues relevant to population persistence as climate changes are the rate, type, magnitude, and spatial pattern of climate-induced abiotic and biotic change; generation time and life history of the organism; extent and type of phenotypic plasticity; amount and distribution of adaptive genetic variation across space and time; dispersal potential; and size and connectivity of subpopulations. An understanding of limits to plasticity and evolutionary potential across traits, populations, and species and feedbacks between adaptive and demographic responses is lacking. Integrated knowledge of coupled ecological and evolutionary mechanisms will increase understanding of the resilience and probabilities of persistence of populations and species.

Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine

Populations are shifting their phenology in response to climate change, but these shifts are often asynchronous among interacting species. Resulting phenological mismatches can drive simultaneous changes in natural selection and population demography, but the links between these interacting processes are poorly understood. Here we analyse 37 years of data from an individual-based study of great tits (Parus major) in the Netherlands and use mixed-effects models to separate the within- and across-year effects of phenological mismatch between great tits and caterpillars (a key food source for developing nestlings) on components of fitness at the individual and population levels. Several components of individual fitness were affected by individual mismatch (i.e. late breeding relative to the caterpillar food peak date), including the probability of double-brooding, fledgling success, offspring recruitment probability and the number of recruits. Together these effects contributed to an overall negative relationship between relative fitness and laying dates, that is, selection for earlier laying on average. Directional selection for earlier laying was stronger in years where birds bred on average later than the food peak, but was weak or absent in years where the phenology of birds and caterpillars matched (i.e. no population mismatch). The mean number of fledglings per female was lower in years when population mismatch was high, in part because fewer second broods were produced. Population mismatch had a weak effect on the mean number of recruits per female, and no effect on mean adult survival, after controlling for the effects of breeding density and the quality of the autumnal beech (Fagus sylvatica) crop. These findings illustrate how climate change-induced mismatch can have strong effects on the relative fitness of phenotypes within years, but weak effects on mean demographic rates across years. We discuss various general mechanisms that influence the extent of coupling between breeding phenology, selection and population dynamics in open populations subject to strong density regulation and stochasticity.

Population growth in a wild bird Is buffered against phenological mismatch

Balancing Act Life cycles are strongly influenced by seasonal and interannual environmental and climate events. Such phenological timings are likely to shift as our climate changes, but species exist in communities, and not all species can be expected to shift in concert. Reed et al. (p. 488) used long-term data on European great tits to reveal how the negative consequences of phenological mismatch can be buffered: Lower fitness in individuals subject to mismatch-driven reductions of food availability was balanced by reductions in competition. Thus, overall, the population is resilient and has not declined. Warmer springtimes have induced great tits to lay their eggs earlier without affecting long-term fitness. Broad-scale environmental changes are altering patterns of natural selection in the wild, but few empirical studies have quantified the demographic cost of sustained directional selection in response to these changes. We tested whether population growth in a wild bird is negatively affected by climate change–induced phenological mismatch, using almost four decades of individual-level life-history data from a great tit population. In this population, warmer springs have generated a mismatch between the annual breeding time and the seasonal food peak, intensifying directional selection for earlier laying dates. Interannual variation in population mismatch has not, however, affected population growth. We demonstrated a mechanism contributing to this uncoupling, whereby fitness losses associated with mismatch are counteracted by fitness gains due to relaxed competition. These findings imply that natural populations may be able to tolerate considerable maladaptation driven by shifting climatic conditions without undergoing immediate declines.

Timing is everything: flexible phenology and shifting selection in a colonial seabird

1. In order to reproduce successfully in a temporally varying environment, iteroparous animals must exhibit considerable behavioural flexibility across their lifetimes. By adjusting timing of breeding each year, parents can ensure optimal overlap between the energy intensive period of offspring production and the seasonal peak in favourable environmental conditions, thereby increasing their chances of successfully rearing young. 2. Few studies investigate variation among individuals in how they respond to fluctuating conditions, or how selection acts on these individual differences, but this information is essential for understanding how populations will cope with rapid environmental change. 3. We explored inter-annual trends in breeding time and individual responses to environmental variability in common guillemots Uria aalge, an important marine top predator in the highly variable California Current System. Complex, nonlinear relationships between phenology and oceanic and climate variables were found at the population level. Using a novel application of a statistical technique called random regression, we showed that individual females responded in a nonlinear fashion to environmental variability, and that reaction norm shape differed among females. 4. The pattern and strength of selection varied substantially over a 34-year period, but in general, earlier laying was favoured. Females deviating significantly from the population mean laying date each year also suffered reduced breeding success, with the strength of nonlinear selection varying in relation to environmental conditions. 5. We discuss our results in the wider context of an emerging literature on the evolutionary ecology of individual-level plasticity in the wild. Better understanding of how species-specific factors and local habitat features affect the timing and success of breeding will improve our ability to predict how populations will respond to climate change.

Responding to environmental change: plastic responses vary little in a synchronous breeder

The impact of environmental change on animal populations is strongly influenced by the ability of individuals to plastically adjust key life-history events. There is therefore considerable interest in establishing the degree of plasticity in traits and how selection acts on plasticity in natural populations. Breeding time is a key life-history trait that affects fitness and recent studies have found that females vary significantly in their breeding time–environment relationships, with selection often favouring individuals exhibiting stronger plastic responses. In contrast, here, we show that although breeding time in the common guillemot, Uria aalge, is highly plastic at the population level in response to a large-scale environmental cue (the North Atlantic Oscillation, NAO), there is very little between-individual variation—most individuals respond to this climate cue very similarly. We demonstrate strong stabilizing selection against individuals who deviate from the average population-level response to NAO. This species differs significantly from those previously studied in being a colonial breeder, in which reproductive synchrony has a substantial impact on fitness; we suggest that counter selection imposed by a need for synchrony could limit individuals in their response and potential for directional selection to act. This demonstrates the importance of considering the relative costs and benefits of highly plastic responses in assessing the likely response of a population to the environmental change.

Time to Evolve? Potential Evolutionary Responses of Fraser River Sockeye Salmon to Climate Change and Effects on Persistence

Evolutionary adaptation affects demographic resilience to climate change but few studies have attempted to project changes in selective pressures or quantify impacts of trait responses on population dynamics and extinction risk. We used a novel individual-based model to explore potential evolutionary changes in migration timing and the consequences for population persistence in sockeye salmon Oncorhynchus nerka in the Fraser River, Canada, under scenarios of future climate warming. Adult sockeye salmon are highly sensitive to increases in water temperature during their arduous upriver migration, raising concerns about the fate of these ecologically, culturally, and commercially important fish in a warmer future. Our results suggest that evolution of upriver migration timing could allow these salmon to avoid increasingly frequent stressful temperatures, with the odds of population persistence increasing in proportion to the trait heritability and phenotypic variance. With a simulated 2°C increase in average summer river temperatures by 2100, adult migration timing from the ocean to the river advanced by ∼10 days when the heritability was 0.5, while the risk of quasi-extinction was only 17% of that faced by populations with zero evolutionary potential (i.e., heritability fixed at zero). The rates of evolution required to maintain persistence under simulated scenarios of moderate to rapid warming are plausible based on estimated heritabilities and rates of microevolution of timing traits in salmon and related species, although further empirical work is required to assess potential genetic and ecophysiological constraints on phenological adaptation. These results highlight the benefits to salmon management of maintaining evolutionary potential within populations, in addition to conserving key habitats and minimizing additional stressors where possible, as a means to build resilience to ongoing climate change. More generally, they demonstrate the importance and feasibility of considering evolutionary processes, in addition to ecology and demography, when projecting population responses to environmental change.

The portfolio concept in ecology and evolution

Biological systems have similarities to efficient financial portfolios; the emergent properties of aggregate systems are often less volatile than their components. These portfolio effects derive from statistical averaging across the dynamics of system components, which often correlate weakly or negatively with each other through time and space. The “portfolio” concept when applied to ecological research provides important insights into how ecosystems are organized, how species interact, and how evolutionary strategies develop. It also helps identify appropriate scales for developing robust management and conservation schemes, and offers an approach that does not rely on prescriptive predictions about threats in an uncertain future. Rather, it presents a framework for managing risk from inevitable perturbations, many of which we will not be able to understand or anticipate.

Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change?

Populations need to adapt to sustained climate change, which requires micro-evolutionary change in the long term. A key question is how the rate of this micro-evolutionary change compares with the rate of environmental change, given that theoretically there is a ‘critical rate of environmental change’ beyond which increased maladaptation leads to population extinction. Here, we parametrize two closely related models to predict this critical rate using data from a long-term study of great tits (Parus major). We used stochastic dynamic programming to predict changes in optimal breeding time under three different climate scenarios. Using these results we parametrized two theoretical models to predict critical rates. Results from both models agreed qualitatively in that even ‘mild’ rates of climate change would be close to these critical rates with respect to great tit breeding time, while for scenarios close to the upper limit of IPCC climate projections the calculated critical rates would be clearly exceeded with possible consequences for population persistence. We therefore tentatively conclude that micro-evolution, together with plasticity, would rescue only the population from mild rates of climate change, although the models make many simplifying assumptions that remain to be tested.