The effect of pregnancy on metabolic scaling and population energy demand in the viviparous fish Gambusia affinis.

Metabolism is a fundamental attribute of all organisms that influences how species affect and are affected by their natural environment. Differences between sexes in ectothermic species may substantially alter metabolic scaling patterns, particularly in viviparous or live-bearing species where females must support their basal metabolic costs and that of their embryos. Indeed, if pregnancy is associated with marked increases in metabolic demand and alters scaling patterns between sexes, this could in turn interact with natural sex ratio variation in nature to affect population-level energy demand. Here, we aimed to understand how sex and pregnancy influence metabolic scaling and how differences between sexes affect energy demand in Gambusia affinis (Western mosquitofish). Using the same method, we measured routine metabolic rate in the field on reproductively active fish and in the laboratory on virgin fish. Our data suggest that changes in energy expenditure related to pregnancy may lead to steeper scaling coefficients in females (b = 0.750) compared to males (b = 0.595). In contrast, virgin females and males had similar scaling coefficients, suggesting negligible sex differences in metabolic costs in reproductively inactive fish. Further, our data suggest that incorporating sex differences in allometric scaling may alter population-level energy demand by as much as 20-28%, with the most pronounced changes apparent in male-biased populations due to the lower scaling coefficient of males. Overall, our data suggest that differences in energy investment in reproduction between sexes driven by pregnancy may alter allometric scaling and population-level energy demand.

Correlated contemporary evolution of life history traits in New Zealand Chinook salmon, Oncorhynchus tshawytscha.

Size at age and age at maturity are important life history traits, affecting individual fitness and population demography. In salmon and other organisms, size and growth rate are commonly considered cues for maturation and thus age at maturity may or may not evolve independently of these features. Recent concerns surrounding the potential phenotypic and demographic responses of populations facing anthropogenic disturbances, such as climate change and harvest, place a premium on understanding the evolutionary genetic basis for evolution in size at age and age at maturity. In this study, we present the findings from a set of common-garden rearing experiments that empirically assess the heritable basis of phenotypic divergence in size at age and age at maturity in Chinook salmon (Oncorhynchus tshawytscha) populations introduced to New Zealand. We found consistent evidence of heritable differences among populations in both size at age and age at maturity, often corresponding to patterns observed in the wild. Populations diverged in size and growth profiles, even when accounting for eventual age at maturation. By contrast, most, but not all, cases of divergence in age at maturity were driven by the differences in size or growth rate rather than differences in the threshold relationship linking growth rate and probability of maturation. These findings help us understand how life histories may evolve through trait interactions in populations exposed to natural and anthropogenic disturbances, and how we might best detect such evolution.

Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies.

Environmental gradients often lead to the parallel evolution of populations and species. To what extent do such gradients also lead to parallel evolution of the sexes? We used guppies (Poecilia reticulata) to examine the parallel and independent (sex-specific) aspects of population divergence in response to predation and habitat features. Geometric morphometrics was used to analyse size and shape variation for 1335 guppies from 27 to 31 sites sampled in each of 2 years. Body size showed strong parallel population divergence; both sexes were larger at sites with a more open canopy and with higher flow. Body shape showed a mixture of parallel and independent population divergence. The strongest and most consistent effects were (1) high-predation sites had males with smaller heads and deeper caudal peduncles, (2) open-canopy sites had females with smaller heads and more distended abdomens and (3) high-flow sites had males and females with smaller heads and deeper caudal peduncles.

Migratory costs and contemporary evolution of reproductive allocation in male chinook salmon.

Energetically demanding migrations may impact the resources available for reproductive trait development and activity, and hence favour evolution of new investment strategies for remaining resources. We conducted a large-scale experiment to evaluate the proximate cost of migration on male reproductive investment in chinook salmon (Oncorhynchus tshawytscha) and contemporary evolution of reproductive allocation. Experimentally induced differences in migratory costs (17 km inland and 17 m elevation vs. 100 km and 430 m) influenced dorsal hump size and upper jaw length, two traits influencing male mating success that are developed during migration. Longer migration also reduced tissue energy reserves available for competition and length of breeding life. Corresponding shifts in the balance between natural and sexual selection appear to have been responsible for heritable population divergence in secondary sexual trait investment, in approximately 26 generations, following colonization of spawning sites with different migratory demands.

Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon.

Newly established or perturbed populations are often the focus of conservation concerns but they pose special challenges for population genetics because drift-migration equilibrium is unlikely. To advance our understanding of the evolution of such populations, we investigated structure and gene flow among populations of chinook salmon that formed via natural straying following introduction to New Zealand in the early 1900s. We examined 11 microsatellite loci from samples collected in several sites and years to address two questions: (i) what population differentiation has arisen in the approximately 30 generations since salmon were introduced to New Zealand, relative to temporal variation within populations; and (ii) what are the approximate effective population sizes and amounts of gene flow in these populations? These questions are routinely addressed in studies of indigenous populations, but less often in the case of new populations and rarely with consideration of equilibrium assumptions. We show that despite the recent introduction, continued gene flow and high temporal variability among samples, detectable population structure has arisen among the New Zealand populations, consistent with their colonization pattern and isolation by geographical distance. Furthermore, we use simple individual-based simulations and estimates of effective population sizes to estimate the effective gene flow among drainages under likely nonequilibrium conditions. Similar methodology may be broadly applicable to other studies of population structure and phenotypic evolution under similar nonequilibrium, high gene flow conditions.

Migratory costs and the evolution of egg size and number in introduced and indigenous salmon populations.

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 (approximately 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.

An introduction to microevolution: rate, pattern, process.

This special issue of Genetica brings together a diverse collection of contributions that examine evolution within and among populations (i.e., microevolution), and the role that microevolution plays in the formation of new species and morphological forms (i.e., macroevolution). Many of the papers present evidence of microevolution occurring over contemporary time frames, further validating the near ubiquity of ongoing evolution in the world around us. Several synthetic reviews of empirical work help to define the conditions under which microevolution is or is not likely to occur. Some of the studies speak directly to current controversies in evolutionary biology, such as the relative roles of determinism and contingency, and the nature of the relationship between microevolution and macroevolution. In general, microevolution seems driven largely by deterministic mechanisms, particularly natural selection, but contingency plays a role in (1) determining whether or not suitable conditions are present for evolution to proceed, and (2) guiding the precise manner by which evolution proceeds. Several theoretical treatments and empirical reviews confirm previous research in showing that microevolutionary processes are at least capable of generating macroevolutionary trends. Macroevolution may indeed reflect microevolution writ large but the pattern by which it arises is perhaps best characterized as microevolution writ in fits and starts.

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 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.

Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced chinook salmon populations.

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.