Andrew G. McAdam

Keeping Pace with Fast Climate Change: Can Arctic Life Count on Evolution?

Abstract Adaptations to the cold and to short growing seasons characterize arctic life, but climate in the Arctic is warming at an unprecedented rate. Will plant and animal populations of the Arctic be able to cope with these drastic changes in environmental conditions? Here we explore the potential contribution of evolution by natural selection to the current response of populations to climate change. We focus on the spring phenology of populations because it is highly responsive to climate change and easy to document across a wide range of species. We show that evolution can be fast and can occur at the time scale of a few decades. We present an example of reproductive phenological change associated with climate change (North American red squirrels in the Yukon), where a detailed analysis of quantitative genetic parameters demonstrates contemporary evolution. We answer a series of frequently asked questions that should help biologists less familiar with evolutionary theory and quantitative genetic methods to think about the role of evolution in current responses of ecological systems to climate change. Our conclusion is that evolution by natural selection is a pertinent force to consider even at the time scale of contemporary climate changes. However, all species may not be equal in their capacity to benefit from contemporary evolution.

Anticipatory reproduction and population growth in seed predators.

Mast seeding, the intermittent, synchronous production of large seed crops by a population of plants, is a well-known example of resource pulses that create lagged responses in successive trophic levels of ecological communities. These lags arise because seed predators are thought capable of increasing reproduction and population size only after the resource pulse is available for consumption. The resulting satiation of predators is a widely cited explanation for the evolution of masting. Our study shows that both American and Eurasian tree squirrels anticipate resource pulses and increase reproductive output before a masting event, thereby increasing population size in synchrony with the resource pulse and eliminating the population lag thought to be universal in resource pulse systems.

MATERNAL EFFECTS AND THE POTENTIAL FOR EVOLUTION IN A NATURAL POPULATION OF ANIMALS

Abstract Maternal effects are widespread and can have dramatic influences on evolutionary dynamics, but their genetic basis has been measured rarely in natural populations. We used cross‐fostering techniques and a long‐term study of a natural population of red squirrels, Tamiasciurus hudsonicus, to estimate both direct (heritability) and indirect (maternal) influences on the potential for evolution. Juvenile growth in both body mass and size had significant amounts of genetic variation (mass h2= 0.10; size h2= 0.33), but experienced large, heritable maternal effects. Growth in body mass also had a large positive covariance between direct and maternal genetic effects. The consideration of these indirect genetic effects revealed a greater than three‐fold increase in the potential for evolution of growth in body mass (h t2= 0.36) relative to that predicted by heritability alone. Simple heritabilities, therefore, may severely underestimate or overestimate the potential for evolution in natural populations of animals.

Life histories of female red squirrels and their contributions to population growth and lifetime fitness

ABSTRACT The potential importance of life history traits to population growth rates has been well explored theoretically but has rarely been documented in wild mammals. In this study we used 18 consecutive years of data from a population of North American red squirrels (Tamiasciurus hudsonicus) in the southwest Yukon, Canada, to examine variation in female life history traits and their consequences for population growth rate. Red squirrels in this population experienced severe juvenile mortality, but survivorship beyond age 2 followed a Type I relationship where the annual survival probability decreased with age. Maximum lifespan was 8 y. Some females initiated breeding as yearlings, but most delayed first breeding until 2 y of age or in some cases even later. Annual reproduction generally involved the production of a single litter averaging 3.1 offspring (range: 1 to 7); however, some females attempted a second litter within a single breeding season, either following reproductive failure or, in rare circumstances, after a successful first breeding attempt. Life table characteristics for the 11 cohorts born between 1987 and 1997 indicated a population growth rate close to zero (r = 0.009). Elasticity analysis as well as individual population projection matrices and lifetime reproductive success data indicated that early survival and not age at first reproduction was most strongly associated with a females contribution to population growth. Lifespan accounted for 83.9% of the variation in population growth rate and was positively correlated with age at first reproduction, such that females who bred as yearlings suffered decreased longevity. Collectively, these results emphasize the importance of female survival and not reproductive output to population growth and lifetime fitness in this system.

LIFETIME SELECTION ON HERITABLE LIFE-HISTORY TRAITS IN A NATURAL POPULATION OF RED SQUIRRELS

Abstract Despite their importance in evolutionary biology, heritability and the strength of natural selection have rarely been estimated in wild populations of iteroparous species or have usually been limited to one particular event during an organisms lifetime. Using an animal‐model restricted maximum likelihood and phenotypic selection models, we estimated quantitative genetic parameters and the strength of lifetime selection on parturition date and litter size at birth in a natural population of North American red squirrels, Tamiasciurus hudsonicus. Litter size at birth and parturition date had low heritabilities (h2= 0.15 and 0.16, respectively). We considered potential effects of temporal environmental covariances between phenotypes and fitness and of spatial environmental heterogeneity in estimates of selection. Selection favored early breeders and females that produced litter sizes close to the population average. Stabilizing selection on litter size at birth may occur because of a trade‐off between number of offspring produced per litter and offspring survival or a trade‐off between a females fecundity and her future reproductive success and survival.

VARIATION IN VIABILITY SELECTION AMONG COHORTS OF JUVENILE RED SQUIRRELS (TAMIASCIURUS HUDSONICUS)

Abstract.— Selection will result in observable changes in traits only if it acts consistently in space and time, but few estimates of selection in natural populations have been temporally replicated. Here we estimate viability selection on nestling growth rates for 13 cohorts (1989–2001) of red squirrels (Tamiasciurus hudsonicus) from a natural population located in southwestern Yukon, Canada. Directional selection on nestling growth rates varied in magnitude and direction from one cohort to the next. The magnitude of directional selection was relatively weak in most years (median (β= 0.24), but there were episodes of very strong viability selection ((β > 0.5) in some cohorts. We found no evidence of significant stabilizing or disruptive selection on this trait. Examination of viability selection episodes over shorter time periods suggested that the strength of selection on juveniles in this population was positively related to the time scale over which selection was measured. Viability selection from birth to emergence from the natal nest (50 days of age) and from emergence to successful recruitment (100 days of age) were positively correlated, but were both independent of selection on nestling growth rates from recruitment to potential breeding age (one year). The strength of directional selection on growth rates prior to recruitment was negatively correlated with spring temperature whereas selection from recruitment to breeding was positively correlated with the abundance of spruce cones produced in the previous fall. Episodes of strong directional selection from birth to breeding age appear to be due to potentially rare combinations of environmental conditions. As a result, predicting the occurrence of very strong episodes of selection will be extremely difficult, but predicting the microevolutionary responses to observed selection on individual cohorts remains feasible.

Fecal cortisol metabolite levels in free-ranging North American red squirrels: Assay validation and the effects of reproductive condition

Patterns in stress hormone (glucocorticoid: GC) levels and their relationship to reproductive condition in natural populations are rarely investigated. In this study, we (1) validate an enzyme-immunoassay to measure fecal cortisol metabolite (FCM) levels in North American red squirrels (Tamiasciurus hudsonicus), and (2) examine relationships between FCM levels and reproductive condition in a free-ranging red squirrel population. Injected radiolabeled cortisol was entirely metabolized and excreted in both the urine (mean+/-SE; 70.3+/-0.02%) and feces (29.7+/-0.02%), with a lag time to peak excretion in the feces of 10.9+/-2.3h. Our antibody reacted with several cortisol metabolites, and an adrenocorticotropic injection significantly increased FCM levels above baseline levels at 8h post-injection. Relative to baseline levels, manipulation by handling also tended to increase FCM levels at 8h post-manipulation, but this difference was not significant. FCM levels did not differ significantly between samples frozen immediately and 5h after collection. Reproductive condition significantly affected FCM levels in free-ranging females (pregnant>lactating>post-lactating>non-breeding) but not males (scrotal testes vs. abdominal testes). Among females with known parturition dates, FCM levels increased during gestation, peaked at parturition, and declined during lactation. The difference between pregnant and lactating females was therefore dependent upon when the fecal samples were obtained during these periods, suggesting caution in categorizing reproductive stages. This study demonstrates the utility of fecal hormone metabolite assays to document patterns of glucocorticoid levels in free-ranging animals.

OXIDATIVE DAMAGE INCREASES WITH REPRODUCTIVE ENERGY EXPENDITURE AND IS REDUCED BY FOOD-SUPPLEMENTATION

A central principle in life‐history theory is that reproductive effort negatively affects survival. Costs of reproduction are thought to be physiologically based, but the underlying mechanisms remain poorly understood. Using female North American red squirrels (Tamiasciurus hudsonicus), we test the hypothesis that energetic investment in reproduction overwhelms investment in antioxidant protection, leading to oxidative damage. In support of this hypothesis we found that the highest levels of plasma protein oxidative damage in squirrels occurred during the energetically demanding period of lactation. Moreover, plasma protein oxidative damage was also elevated in squirrels that expended the most energy and had the lowest antioxidant protection. Finally, we found that squirrels that were food‐supplemented during lactation and winter had increased antioxidant protection and reduced plasma protein oxidative damage providing the first experimental evidence in the wild that access to abundant resources can reduce this physiological cost.

The functional response of a hoarding seed predator to mast seeding.

Mast seeding involves the episodic and synchronous production of large seed crops by perennial plants. The predator satiation hypothesis proposes that mast seeding maximizes seed escape because seed predators consume a decreasing proportion of available seeds with increasing seed production. However, the seed escape benefits of masting depend not only on whether predators are satiated at high levels of seed production, but also on the shape of their functional response (type II vs. type III), and the actual proportion of available seeds that they consume at different levels of seed production. North American red squirrels (Tamiasciurus hudsonicus) are the primary vertebrate predator of white spruce (Picea glauca) mast seed crops in many boreal regions because they hoard unopened cones in underground locations, preempting the normal sequence of cone opening, seed dispersal, and seed germination. We document the functional response of cone-hoarding by red squirrels across three non-mast years and one mast year by estimating the number of cones present in the territories of individual red squirrels and the proportion of these cones that they hoarded each autumn. Even though red squirrels are not constrained by the ingestive and on-body (fat reserves) energy reserve limitations experienced by animals that consume seeds directly, most squirrels hoarded < 10% of the cones present on their territories under mast conditions. Cone availability during non-mast years also reached levels that satiated the hoarding activity of red squirrels; however, this occurred only on the highest-quality territories. Squirrels switched to mushroom-hoarding when cone production was low and mushrooms were abundant. This resulted in type III functional response whereby the proportional harvest of cones was highest at levels of cone availability that were intermediate within non-mast years. Overall, more cones escaped squirrel cone-hoarding during a mast event than when cone production was low in non-mast years, which supports the predator satiation hypothesis. However, the highly variable seed escape in non-mast years may help to explain why all spruce cone production is not concentrated into fewer, larger, mast years.

Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels.

Sources of variation in growth in body mass were assessed in natural and experimental conditions of high and low food abundance using reciprocal cross‐fostering techniques and long‐term data (1987–2002) for a population of North American red squirrels (Tamiasciurus hudsonicus). Growth rates were significantly higher in naturally good and food supplemented conditions, than in poor conditions. Mother–offspring resemblance was higher in poor conditions as a result of large increases in both the direct genetic variance and direct‐maternal genetic covariance and a smaller increase in the coefficient of maternal variation. Furthermore, the genetic correlation across environments was significantly less than one indicating that sources of heritable variation differed between the two environments. These results are consistent with the hypothesis that selection has eroded heritable variation for growth more in good conditions and indicate the potential for independent adaptation of growth rates in good and poor conditions.