Anna Kuparinen

Long‐distance gene flow and adaptation of forest trees to rapid climate change

Forest trees are the dominant species in many parts of the world and predicting how they might respond to climate change is a vital global concern. Trees are capable of long-distance gene flow, which can promote adaptive evolution in novel environments by increasing genetic variation for fitness. It is unclear, however, if this can compensate for maladaptive effects of gene flow and for the long-generation times of trees. We critically review data on the extent of long-distance gene flow and summarise theory that allows us to predict evolutionary responses of trees to climate change. Estimates of long-distance gene flow based both on direct observations and on genetic methods provide evidence that genes can move over spatial scales larger than habitat shifts predicted under climate change within one generation. Both theoretical and empirical data suggest that the positive effects of gene flow on adaptation may dominate in many instances. The balance of positive to negative consequences of gene flow may, however, differ for leading edge, core and rear sections of forest distributions. We propose future experimental and theoretical research that would better integrate dispersal biology with evolutionary quantitative genetics and improve predictions of tree responses to climate change.

Spread of North American wind-dispersed trees in future environments.

Despite ample research, understanding plant spread and predicting their ability to track projected climate changes remain a formidable challenge to be confronted. We modelled the spread of North American wind-dispersed trees in current and future (c. 2060) conditions, accounting for variation in 10 key dispersal, demographic and environmental factors affecting population spread. Predicted spread rates vary substantially among 12 study species, primarily due to inter-specific variation in maturation age, fecundity and seed terminal velocity. Future spread is predicted to be faster if atmospheric CO(2) enrichment would increase fecundity and advance maturation, irrespective of the projected changes in mean surface windspeed. Yet, for only a few species, predicted wind-driven spread will match future climate changes, conditioned on seed abscission occurring only in strong winds and environmental conditions favouring high survival of the farthest-dispersed seeds. Because such conditions are unlikely, North American wind-dispersed trees are expected to lag behind the projected climate range shift.

Mechanistic models of seed dispersal by wind

Over the past century, various mechanistic models have been developed to estimate the magnitude of seed dispersal by wind, and to elucidate the relative importance of physical and biological factors affecting this passive transport process. The conceptual development has progressed from ballistic models, through models incorporating vertically variable mean horizontal windspeed and turbulent excursions, to models accounting for discrepancies between airflow and seed motion. Over hourly timescales, accounting for turbulent fluctuations in the vertical velocity component generally leads to a power-law dispersal kernel that is censored by an exponential cutoff far from the seed source. The parameters of this kernel vary with the flow field inside the canopy and the seed terminal velocity. Over the timescale of a dispersal season, with mean wind statistics derived from an “extreme-value” distribution, these distribution-tail effects are compounded by turbulent diffusion to yield seed dispersal distances that are two to three orders of magnitude longer than the corresponding ballistic models. These findings from analytic models engendered explicit simulations of the effects of turbulence on seed dispersal using computationally intensive fluid dynamics tools. This development marks a bifurcation in the approaches to wind dispersal, seeking either finer resolution of the dispersal mechanism at the scale of a single dispersal event, or mechanistically derived analytical dispersal kernels needed to resolve long-term and large-scale processes such as meta-population dynamics and range expansion. Because seed dispersal by wind is molded by processes operating over multiple scales, new insights will require novel theoretical tactics that blend these two approaches while preserving the key interactions across scales.

Life‐history correlates of extinction risk and recovery potential

Extinction risk is inversely associated with maximum per capita population growth rate (r(max)). However, this parameter is not known for most threatened species, underscoring the value in identifying correlates of r(max) that, in the absence of demographic data, would indirectly allow one to identify species and populations at elevated risk of extinction and their associated recovery potential. We undertook a comparative life-history analysis of 199 species from three taxonomic classes: Chondrichthyes (e.g., sharks; n = 82), Actinopterygii (teleost or bony fishes; n = 47), and Mammalia (n = 70, including 16 marine species). Median r(max) was highest for (and similar between) terrestrial mammals (0.71) and teleosts (0.43), significantly lower among chondrichthyans (0.26), and lower still in marine mammals (0.07). Age at maturity was the primary (and negative) correlate of r(max). In contrast, although body size was negatively correlated with r(max) in chondrichthyans and mammals, evidence of an association in teleosts was equivocal, and fecundity was not related to r(max) in fishes, despite recurring assertions to the contrary. Our analyses suggest that age at maturity can serve as a universal predictor of extinction risk in fishes and mammals when r(max) itself is unknown. Moreover, in contrast to what is generally expected, the recovery potential of teleost fishes does not differ from that of terrestrial mammals. Our findings are supportive of the application of extinction-risk criteria that are based on generation time and that are independent of taxonomic affinity.

Consequences of fisheries-induced evolution for population productivity and recovery potential

Fisheries-induced evolution has become a major branch of the research on anthropogenic and contemporary evolution. Within the conservation context, fisheries-induced evolution has been hypothesized to negatively affect the persistence and recovery potential of depleted populations, but this has not been explicitly investigated. Here, we investigate how fisheries-induced evolution of Atlantic cod (Gadus morhua L.) life histories affects per capita population growth rate, a parameter negatively correlated with extinction risk. We simulate the evolutionary and ecological dynamics of a cod population for a 100 year period of size-selective harvesting, followed thereafter by 300 years of recovery. To evaluate the relative importance of harvest-induced evolution, we either allowed life histories to evolve during and after the fishing period, or we assumed that fisheries-induced evolution was absent. Population growth rates did not differ appreciably between the evolutionary and non-evolutionary simulation scenarios, despite the emergence of rather pronounced differences in life histories. The underlying reason was that in the absence of fishing the cumulative lifetime reproductive outputs were very similar among differing life histories. The results suggest that fisheries-induced evolution might not always have as clear-cut an effect on population growth rate as previously anticipated.

Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact.

Humans are changing marine ecosystems worldwide, both directly through fishing and indirectly through climate change. One of the little explored outcomes of human-induced change involves the decreasing body sizes of fishes. We use a marine ecosystem model to explore how a slow (less than 0.1% per year) decrease in the length of five harvested species could affect species interactions, biomasses and yields. We find that even small decreases in fish sizes are amplified by positive feedback loops in the ecosystem and can lead to major changes in natural mortality. For some species, a total of 4 per cent decrease in length-at-age over 50 years resulted in 50 per cent increase in predation mortality. However, the magnitude and direction in predation mortality changes differed among species and one shrinking species even experienced reduced predation pressure. Nevertheless, 50 years of gradual decrease in body size resulted in 1–35% decrease in biomasses and catches of all shrinking species. Therefore, fisheries management practices that ignore contemporary life-history changes are likely to overestimate long-term yields and can lead to overfishing.

The evolutionary legacy of size-selective harvesting extends from genes to populations.

Size‐selective harvesting is assumed to alter life histories of exploited fish populations, thereby negatively affecting population productivity, recovery, and yield. However, demonstrating that fisheries‐induced phenotypic changes in the wild are at least partly genetically determined has proved notoriously difficult. Moreover, the population‐level consequences of fisheries‐induced evolution are still being controversially discussed. Using an experimental approach, we found that five generations of size‐selective harvesting altered the life histories and behavior, but not the metabolic rate, of wild‐origin zebrafish (Danio rerio). Fish adapted to high positively size selective fishing pressure invested more in reproduction, reached a smaller adult body size, and were less explorative and bold. Phenotypic changes seemed subtle but were accompanied by genetic changes in functional loci. Thus, our results provided unambiguous evidence for rapid, harvest‐induced phenotypic and evolutionary change when harvesting is intensive and size selective. According to a life‐history model, the observed life‐history changes elevated population growth rate in harvested conditions, but slowed population recovery under a simulated moratorium. Hence, the evolutionary legacy of size‐selective harvesting includes populations that are productive under exploited conditions, but selectively disadvantaged to cope with natural selection pressures that often favor large body size.

Increases in air temperature can promote wind-driven dispersal and spread of plants

Long-distance dispersal (LDD) of seeds and pollen shapes the spatial dynamics of plant genotypes, populations and communities. Quantifying LDD is thus important for predicting the future dynamics of plants exposed to environmental changes. However, environmental changes can also alter the behaviour of LDD vectors: for instance, increasing air temperature may enhance atmospheric instability, thereby altering the turbulent airflow that transports seed and pollen. Here, we investigate temperature effects on wind dispersal in a boreal forest using a 10-year time series of micrometeorological measurements and a Lagrangian stochastic model for particle transport. For a wide range of dispersal and life history types, we found positive relations between air temperature and LDD. This translates into a largely consistent positive effect of +3°C warming on predicted LDD frequencies and spread rates of plants. Relative increases in LDD frequency tend to be higher for heavy-seeded plants, whereas absolute increases in LDD and spread rates are higher for light-seeded plants for which wind is often an important dispersal vector. While these predicted increases are not sufficient to compensate forecasted range losses and environmental changes can alter plant spread in various ways, our results generally suggest that warming can promote wind-driven movements of plant genotypes and populations in boreal forests.

Estimating fisheries-induced selection: traditional gear selectivity research meets fisheries-induced evolution

The study of fisheries‐induced evolution is a research field which is becoming recognized both as an important and interesting problem in applied evolution, as well as a practical management problem in fisheries. Much of the research in fisheries‐induced evolution has focussed on quantifying and proving that an evolutionary response has taken place, but less effort has been invested on the actual processes and traits underlying capture of a fish by a fishing gear. This knowledge is not only needed to understand possible phenotypic selection associated to fishing but also to help to device sustainable fisheries and management strategies. Here, we draw attention to the existing knowledge about selectivity of fishing gears and outline the ways in which this information could be utilized in the context of fisheries‐induced evolution. To these ends, we will introduce a mathematical framework commonly applied to quantify fishing gear selectivity, illustrate the link between gear selectivity and the change in the distribution of phenotypes induced by fishing, review what is known about selectivity of commonly used fishing gears, and discuss how this knowledge could be applied to improve attempts to predict evolutionary impacts of fishing.

How fast is fisheries-induced evolution? Quantitative analysis of modelling and empirical studies

A number of theoretical models, experimental studies and time‐series studies of wild fish have explored the presence and magnitude of fisheries‐induced evolution (FIE). While most studies agree that FIE is likely to be happening in many fished stocks, there are disagreements about its rates and implications for stock viability. To address these disagreements in a quantitative manner, we conducted a meta‐analysis of FIE rates reported in theoretical and empirical studies. We discovered that rates of phenotypic change observed in wild fish are about four times higher than the evolutionary rates reported in modelling studies, but correlation between the rate of change and instantaneous fishing mortality (F) was very similar in the two types of studies. Mixed‐model analyses showed that in the modelling studies traits associated with reproductive investment and growth evolved slower than rates related to maturation. In empirical observations age‐at‐maturation was changing faster than other life‐history traits. We also found that, despite different assumption and modelling approaches, rates of evolution for a given F value reported in 10 of 13 modelling studies were not significantly different.