Michael T. Kinnison

Contemporary evolution meets conservation biology

Recent research has revealed that evolution often occurs on contemporary timescales, often within decades. Contemporary evolution is associated with the same factors that are driving the current extinction crisis: habitat loss and degradation, overharvesting and exotic species. Thus, it is relevant to many conservation situations. First, habitat fragmentation might influence the potential of a population to adapt in response environmental degradation. Second, certain harvesting strategies can result in the evolution of life-history traits, ultimately resulting in negative impacts on harvestable yield. Third, the establishment of exotic species can be influenced by their adaptive potential and our ability to limit that potential. Furthermore, contemporary evolution is of concern for intensively managed species, because it might reduce their fitness in native habitats. Ultimately, contemporary evolution is influenced by complex interactions among population size, genetic variation, the strength of selection, and gene flow, making most management scenarios unique. In a world filled with contemporary evolution, conservation efforts that ignore its implications will be less efficient and perhaps even risk prone. Humans have become an evolutionary force of extraordinary influence [1], evidenced most obviously by an unprecedented extinction rate that is attributable to their activities [2]. Human activities are also associated with evolutionary changes that can occur within a few hundred years, otherwise known as CONTEMPORARY EVOLUTION (see Glossary) [3‐5].

PERSPECTIVE: THE PACE OF MODERN LIFE: MEASURING RATES OF CONTEMPORARY MICROEVOLUTION

We evaluate methods for measuring and specifying rates of microevolution in the wild, with particular regard to studies of contemporary, often deemed “rapid,” evolution. A considerable amount of ambiguity and inconsistency persists within the field, and we provide a number of suggestions that should improve study design, inference, and clarity of presentation. (1) Some studies measure change over time within a population (allochronic) and others measure the difference between two populations that had a common ancestor in the past (synchronic). Allochronic studies can be used to estimate rates of “evolution,” whereas synchronic studies more appropriately estimate rates of “divergence.” Rates of divergence may range from a small fraction to many times the actual evolutionary rates in the component populations. (2) Some studies measure change using individuals captured from the wild, whereas others measure differences after rearing in a common environment. The first type of study can be used to specify “phenotypic” rates and the later “genetic” rates. (3) The most commonly used evolutionary rate metric, the darwin, has a number of theoretical shortcomings. Studies of microevolution would benefit from specifying rates in standard deviations per generation, the haldane. (4) Evolutionary rates are typically specified without an indication of their precision. Readily available methods for specifying confidence intervals and statistical significance (regression, bootstrapping, randomization) should be implemented. (5) Microevolutionists should strive to accumulate time series, which can reveal temporal shifts in the rate of evolution and can be used to identify evolutionary patterns. (6) Evolutionary rates provide a convenient way to compare the tempo of evolution across studies, traits, taxa, and time scales, but such comparisons are subject to varying degrees of confidence. Comparisons across different time scales are particularly tenuous. (7) A number of multivariate rate measures exist, but considerable theoretical development is required before their utility can be determined. We encourage the continued investigation of evolutionary rates because the information they provide is relevant to a wide range of theoretical and practical issues.

Human influences on rates of phenotypic change in wild animal populations

Human activities can expose populations to dramatic environmental perturbations, which may then precipitate adaptive phenotypic change. We ask whether or not phenotypic changes associated with human‐disturbed (anthropogenic) contexts are greater than those associated with more ‘natural’ contexts. Our meta‐analysis is based on more than 3000 rates of phenotypic change in 68 ‘systems’, each representing a given species in a particular geographical area. We find that rates of phenotypic change are greater in anthropogenic contexts than in natural contexts. This difference may be influenced by phenotypic plasticity — because it was evident for studies of wild‐caught individuals (which integrate both genetic and plastic effects) but not for common‐garden or quantitative genetic studies (which minimize plastic effects). We also find that phenotypic changes in response to disturbance can be remarkably abrupt, perhaps again because of plasticity. In short, humans are an important agent driving phenotypic change in contemporary populations. Although these changes sometimes have a genetic basis, our analyses suggest a particularly important contribution from phenotypic plasticity.

Human predators outpace other agents of trait change in the wild

The observable traits of wild populations are continually shaped and reshaped by the environment and numerous agents of natural selection, including predators. In stark contrast with most predators, humans now typically exploit high proportions of prey populations and target large, reproductive-aged adults. Consequently, organisms subject to consistent and strong ‘harvest selection’ by fishers, hunters, and plant harvesters may be expected to show particularly rapid and dramatic changes in phenotype. However, a comparison of the rate at which phenotypic changes in exploited taxa occurs relative to other systems has never been undertaken. Here, we show that average phenotypic changes in 40 human-harvested systems are much more rapid than changes reported in studies examining not only natural (n = 20 systems) but also other human-driven (n = 25 systems) perturbations in the wild, outpacing them by >300% and 50%, respectively. Accordingly, harvested organisms show some of the most abrupt trait changes ever observed in wild populations, providing a new appreciation for how fast phenotypes are capable of changing. These changes, which include average declines of almost 20% in size-related traits and shifts in life history traits of nearly 25%, are most rapid in commercially exploited systems and, thus, have profound conservation and economic implications. Specifically, the widespread potential for transitively rapid and large effects on size- or life history-mediated ecological dynamics might imperil populations, industries, and ecosystems.

The pace of modern life II: From rates of contemporary microevolution to pattern and process

We compiled a database of microevolution on contemporary time scales in nature (47 source articles; 30 animal species), comprising 2649 evolutionary rates in darwins (proportional change per million years) and 2151 evolutionary rates in haldanes (standard deviations per generation). Here we demonstrate how quantitative rate measures can provide general insights into patterns and processes of evolution. The frequency distribution of evolutionary rates was approximately log-normal, with many slow rates and few fast rates. Net selection intensities estimated from haldanes were on average lower than selection intensities commonly measured directly in natural populations. This difference suggests that natural selection could easily accomplish observed microevolution but that the intensities of selection typically measured in nature are rarely maintained for long (otherwise observed evolutionary rates would be higher). Traits closely associated with fitness (life history traits) appear to evolve at least as fast as traits less closely tied to fitness (morphology). The magnitude of evolutionary difference increased with the length of the time interval, particularly when maximum rates from a given study were considered. This pattern suggests a general underlying tendency toward increasing evolutionary diversification with time. However, evolutionary rates also tended to decrease with time, perhaps because longer time intervals average increasingly disparate rates over time, or because evolution slows when populations approach new optima or as genetic variation is depleted. In combination, our results suggest that macroevolutionary transitions may ultimately arise through microevolution occasionally ‘writ large’ but are perhaps temporally characterized by microevolution ‘writ in fits and starts’.

EVOLUTION OF TEMPORAL ISOLATION IN THE WILD: GENETIC DIVERGENCE IN TIMING OF MIGRATION AND BREEDING BY INTRODUCED CHINOOK SALMON POPULATIONS

Abstract. The timing of migration and breeding are key life‐history traits; they are not only adaptations of populations to their environments, but can serve to increase reproductive isolation, facilitating further divergence among populations. As part of a study of divergence of chinook salmon, Oncorhynchus tshawytscha, populations, established in New Zealand from a common source in the early 1900s, we tested the hypotheses that the timing of migration and breeding are under genetic control and that the populations genetically differ in these traits despite phenotypic overlap in timing in the wild. Representatives of families from two populations were collected within a day or two of each other, reared in a common environment, and then released to sea from each of two different rivers, while other family representatives were retained in fresh water to maturity. The date of maturation of fish held in fresh water and the dates of return from the ocean and maturation of fish released to sea all showed significant differences between the two populations and among families within populations. The very high heritabilities and genetic correlations estimated for migration and maturation date indicated that these traits would respond rapidly to selection. Combined with the results of related studies on these chinook salmon populations, it appears that spawning time may not only evolve during the initial phases of divergence, but it may play an important role in accelerating divergence in other traits.

The relative influence of natural selection and geography on gene flow in guppies

Two general processes may influence gene flow among populations. One involves divergent selection, wherein the maladaptation of immigrants and hybrids impedes gene flow between ecological environments (i.e. ecological speciation). The other involves geographic features that limit dispersal. We determined the relative influence of these two processes in natural populations of Trinidadian guppies (Poecilia reticulata). If selection is important, gene flow should be reduced between different selective environments. If geography is important, gene flow should be impeded by geographic distance and physical barriers. We examined how genetic divergence, long‐term gene flow, and contemporary dispersal within a watershed were influenced by waterfalls, geographic distance, predation, and habitat features. We found that waterfalls and geographic distance increased genetic divergence and reduced dispersal and long‐term gene flow. Differences in predation or habitat features did not influence genetic divergence or gene flow. In contrast, differences in predation did appear to reduce contemporary dispersal. We suggest that the standard predictions of ecological speciation may be heavily nuanced by the mating behaviour and life history strategies of guppies.

MIGRATORY COSTS AND THE EVOLUTION OF EGG SIZE AND NUMBER IN INTRODUCED AND INDIGENOUS SALMON POPULATIONS

Abstract.— The trade‐off between reproductive investment and migration should be an important factor shaping the evolution of life‐history traits among populations following their radiation into habitats with different migratory costs and benefits. An experimentally induced difference in migratory rigor for families of chinook salmon (Oncorhynchus tshawytscha), of approximately 86 km and 413 m elevation, exacted a cost to somatic energy reserves (∼ 17% reduction in metabolizable mass) and ovarian investment (13.7% reduction in ovarian mass). This cost was associated with a reduction in egg size and paralleled the phenotypic pattern of divergence between two introduced New Zealand populations of common origin, presently breeding at sites with different migration distances. The genetic pattern of divergence of these same populations, detected under common rearing, was consistent with compensation for migratory costs (the population that migrates farther invested more in ovarian mass), but egg number more than egg size was associated with this evolution. These evolutionary patterns are consistent with what is known of the inheritance of these traits and with trade‐offs and constraints favoring initial evolution in offspring number over offspring size. Analysis of egg number‐size patterns of other Pacific salmon populations in their native range supported the hypothesis that migration strongly influences patterns of reproductive allocation, favoring a higher ratio of egg number to egg size with greater migration distance.

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.

Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern, rate, and process

Chinook salmon, Oncorhynchus tshawytscha, from the Sacramento River, California, USA were introduced to New Zealand between 1901 and 1907, and colonized most of their present-day range within about 10 years. The New Zealand populations now vary in phenotypic traits typically used to differentiate salmon populations within their natural range: growth in freshwater and at sea, age at maturity, dates of return to fresh water and reproduction, morphology, and reproductive allocation. This paper reviews a large research program designed to determine the relative contributions of phenotypic plasticity and genetic adaptation to this variation, in an effort to understand the processes underlying the natural evolution of new populations. We found strong evidence of trait divergence between populations within at most 30 generations, particularly in freshwater growth rate, date of return, and reproductive output, with plausible adaptive bases for these differences. Importantly, we also demonstrated not only a genetic basis for post-release survival but higher survival, and hence fitness, of a population released from its established site compared to another population released from the same site. We conclude that divergence of salmon in different rivers probably resulted initially from phenotypic plasticity (e.g., habitat-specific growth rates, and effects of upriver migration on ovarian investment). Philopatry (homing to natal streams) combined with rapid evolution of distinct breeding periods to restrict gene flow, facilitating divergence in other traits. We also suggest that in addition to genetic divergence resulting from random founder effects, divergence may also arise during the very early stages of colonization when the original colonists are a non-random, pre-adapted subset of the source population. This ‘favored founders effect’ immediately improves the fitness of the new population. Overall, this research reveals the complex interplay of environmental and genetic controls over behavior, physiology and life history that characterize the early stages of population differentiation, a process that has taken place repeatedly during the history of salmon populations.