Tarmo Ketola

The Good‐Genes and Compatible‐Genes Benefits of Mate Choice

Genetic benefits from mate choice could be attained by choosing mates with high heritable quality (“good genes”) and that are genetically compatible (“compatible genes”). We clarify the conceptual and empirical framework for estimating genetic benefits of mate choice, stressing that benefits must be measured from offspring fitness because there are no unequivocal surrogates for genetic quality of individuals or for compatibility of parents. We detail the relationship between genetic benefits and additive and nonadditive genetic variance in fitness, showing that the benefits have been overestimated in previous verbal treatments. We point out that additive benefits readily arise from nonadditive gene action and that the idea of “heritable nonadditive benefits” is a misconception. We review the empirical evidence of the magnitude of benefits of good genes and compatible genes in animal populations, and we outline the most promising future directions for empirical research on the genetic benefits of mate choice.

Inbreeding, energy use and condition

In energetic terms, fitness may be seen to be dependent on successful allocation of energy between life‐history traits. In addition, fitness will be constrained by the energy allocation ability, which has also been defined as condition. We suggest here that the allocation ability, estimated as the difference between total energy budget and maintenance metabolism, may be used as a measure of condition. We studied this possibility by measuring the resting metabolic rate and metabolism during forced exercise in Gryllodes sigillatus crickets. To verify that these metabolic traits are closely related to fitness, we experimentally manipulated the degree of inbreeding of individuals belonging to the same pedigree, hence enabling analysis of both inbreeding depression and heritability of traits. We found that inbreeding increased maintenance metabolism, whereas total energy budget was rather insensitive to inbreeding. Despite this, inbreeding led to decreased allocation ability. Overall, metabolic traits exhibited strong inbreeding depression and rather low heritabilities, a pattern that is typical of traits under strong selection. However, traditionally used condition indices were not affected by inbreeding and did not covary with metabolic traits. Moreover, in contrast to the common, but largely untested, tenet, it seems that high resting metabolic rate is indicative of low rather than high quality.

FLUCTUATING TEMPERATURE LEADS TO EVOLUTION OF THERMAL GENERALISM AND PREADAPTATION TO NOVEL ENVIRONMENTS

Environmental fluctuations can select for generalism, which is also hypothesized to increase organisms’ ability to invade novel environments. Here, we show that across a range of temperatures, opportunistic bacterial pathogen Serratia marcescens that evolved in fluctuating temperature (daily variation between 24°C and 38°C, mean 31°C) outperforms the strains that evolved in constant temperature (31°C). The growth advantage was also evident in novel environments in the presence of parasitic viruses and predatory protozoans, but less clear in the presence of stressful chemicals. Adaptation to fluctuating temperature also led to reduced virulence in Drosophila melanogaster host, which suggests that generalism can still be costly in terms of reduced fitness in other ecological contexts. While supporting the hypothesis that evolution of generalism is coupled with tolerance to several novel environments, our results also suggest that thermal fluctuations driven by the climate change could affect both species’ invasiveness and virulence.

Gene expression centroids that link with low intrinsic aerobic exercise capacity and complex disease risk

A strong link exists between low aerobic exercise capacity and complex metabolic diseases. To probe this linkage, we utilized rat models of low and high intrinsic aerobic endurance running capacity that differ also in the risk for metabolic syndrome. We investigated in skeletal muscle gene‐phenotype relationships that connect aerobic endurance capacity with metabolic disease risk factors. The study compared 12 high capacity runners (HCRs) and 12 low capacity runners (LCRs) from generation 18 of selection that differed by 615% for maximal treadmill endurance running capacity. On average, LCRs were heavier and had increased blood glucose, insulin, and triglycerides compared with HCRs. HCRs were higher for resting metabolic rate, voluntary activity, serum high density lipoproteins, muscle capillarity, and mitochondrial area. Bioinformatic analysis of skeletal muscle gene expression data revealed that many genes up‐regulated in HCRs were related to oxidative energy metabolism. Seven mean mRNA expression centroids, including oxidative phosphorylation and fatty acid metabolism, correlated significantly with several exercise capacity and disease risk phenotypes. These expression‐phenotype correlations, together with diminished skeletal muscle capillarity and mitochondrial area in LCR rats, support the general hypothesis that an inherited intrinsic aerobic capacity can underlie disease risks.—Kivelä, R., Silvennoinen, M., Lehti, M., Rinnankoski‐Tuikka, R., Purhonen, T., Ketola, T., Pullinen, K., Vuento, M., Mutanen, N., Sartor, M. A., Reunanen, H., Koch, L. G., Britton, S. L., Kainulainen, H. Gene expression centroids that link with low intrinsic aerobic exercise capacity and complex disease risk. FASEB J. 24, 4565–4574 (2010). www.fasebj.org

Evolution of Hsp90 expression in Tetrahymena thermophila (Protozoa, Ciliata) populations exposed to thermally variable environments.

Abstract Evolutionary consequences of thermally varying environments were studied in the ciliated protozoan Tetrahymena thermophila. Replicated lines were propagated for 60 days, a maximum of 500 generations, in stable, slowly fluctuating (red spectrum), and rapidly fluctuating (blue spectrum) temperatures. The red and blue fluctuations had a dominant period length of 15 days and two hours, respectively. The mean temperature of all time series was 25°C and the fluctuating temperatures had the same minimum (10°C), maximum (40°C), and variance. During the experiment, population sizes and biomasses were monitored at three‐day intervals. After the experiment, carrying capacity and maximum growth rate were measured at low (15°C), intermediate (25°C), and high (35°C) temperatures for each experimental line. Physiological changes in the lines were assessed by measuring the expression of stress‐induced heat shock protein Hsp90 at 25°C, 35°C, and 39°C. Population sizes and biomasses showed no differences between stable, blue, or red temperature treatments during the experiment. Also, after the experiment, mean carrying capacities and maximum growth rates were comparable in the stable, blue, and red temperature treatments. The expression of Hsp90 was higher in lines from the blue environment than in lines from the stable environment. Lines from the red environment had an intermediate level of Hsp90 expression. This supports the hypothesis that inducible thermotolerance and expression of canalizing genes can evolve in response to rapidly varying environments. Furthermore, we found correlative evidence of benefits and disadvantages of high Hsp90 expression. Lines with high expression of Hsp90 had an increased growth rate at the highest temperature when food resources were not limiting growth. At low and intermediate temperatures the same lines had the lowest carrying capacities.

Inbreeding, energy use and sexual signaling

Genetic quality and energy metabolism are expected to have an effect on the level of energetically costly sexual signaling. To explore this we manipulated genetic quality of male decorated crickets (Gryllodes sigillatus) by inbreeding and measured the resting metabolic rate and total energy budget of males. We also measured several aspects of the sexual signaling of males: probability to initiate calling, latency, amount of call bouts, first call bout duration, mean call bout duration and total time spent calling. Inbreeding increased the latency and lowered the first and mean call bout duration. Moreover, the resting metabolic rate had a positive effect, and body mass a negative effect on first call bout duration and mean call bout duration. Our results, suggest that sexual signals are indicative of genetic quality but are also dependent on the physical properties of individuals.

Experimental evolution in fluctuating environments: tolerance measurements at constant temperatures incorrectly predict the ability to tolerate fluctuating temperatures.

The ability to predict the consequences of fluctuating environments on species distribution and extinction often relies on determining the tolerances of species or genotypes in different constant environments (i.e. determining tolerance curves). However, very little is known about the suitability of measurements made in constant environments to predict the level of adaptation to rapidly fluctuating environments. To explore this question, we used bacterial clones adapted to constant or fluctuating temperatures and found that measurements across a range of constant temperatures did not indicate any adaptation to fluctuating temperatures. However, adaptation to fluctuating temperatures was only apparent if growth was measured during thermal fluctuation. Thus, tolerance curves based on measurements in constant environments can be misleading in predicting the ability to tolerate fast environmental fluctuations. Such complications could lead to false estimates of the genetic merits of genotypes and extinction risks of species due to climate change‐induced thermal fluctuations.

Constant, cycling, hot and cold thermal environments: strong effects on mean viability but not on genetic estimates

It has frequently been suggested that trait heritabilities are environmentally sensitive, and there are genetic trade‐offs between tolerating different environments such as hot and cold or constant and fluctuating temperatures. Future climate predictions suggest an increase in both temperatures and their fluctuations. How species will respond to these changes is uncertain, particularly as there is a lack of studies which compare genetic performances in constant vs. fluctuating environments. In this study, we used a nested full‐sib/half‐sib breeding design to examine how the genetic variances and heritabilities of egg‐to‐adult viability differ at high and low temperatures with and without daily fluctuations in temperatures using Drosophila melanogaster as a model organism. Although egg‐to‐adult viability was clearly sensitive to developmental temperatures, heritabilities were not particularly sensitive to developmental temperatures. Moreover, we found that egg‐to‐adult viabilities at different developmental temperatures were positively correlated, suggesting a common genetic background for egg‐to‐adult viability at different temperatures. Finding both a uniform genetic background coupled with rather low heritabilities insensitive to temperatures, our results suggest evolutionary responses are unlikely to be limited by temperature effects on genetic parameters or negative genetic correlations, but by the direct effects of stressful temperatures on egg‐to‐adult viability accompanied with low heritabilities.

Intensive aquaculture selects for increased virulence and interference competition in bacteria

Although increased disease severity driven by intensive farming practices is problematic in food production, the role of evolutionary change in disease is not well understood in these environments. Experiments on parasite evolution are traditionally conducted using laboratory models, often unrelated to economically important systems. We compared how the virulence, growth and competitive ability of a globally important fish pathogen, Flavobacterium columnare, change under intensive aquaculture. We characterized bacterial isolates from disease outbreaks at fish farms during 2003–2010, and compared F. columnare populations in inlet water and outlet water of a fish farm during the 2010 outbreak. Our data suggest that the farming environment may select for bacterial strains that have high virulence at both long and short time scales, and it seems that these strains have also evolved increased ability for interference competition. Our results are consistent with the suggestion that selection pressures at fish farms can cause rapid changes in pathogen populations, which are likely to have long-lasting evolutionary effects on pathogen virulence. A better understanding of these evolutionary effects will be vital in prevention and control of disease outbreaks to secure food production.

DOES ENVIRONMENTAL ROBUSTNESS PLAY A ROLE IN FLUCTUATING ENVIRONMENTS

Fluctuating environments are expected to select for individuals that have highest geometric fitness over the experienced environments. This leads to the prediction that genetically determined environmental robustness in fitness, and average fitness across environments should be positively genetically correlated to fitness in fluctuating environments. Because quantitative genetic experiments resolving these predictions are missing, we used a full‐sib, half‐sib breeding design to estimate genetic variance for egg‐to‐adult viability in Drosophila melanogaster exposed to two constant or fluctuating temperatures that were above the species’ optimum temperature, during development. Viability in two constant environments (25°C or 30°C) was used to estimate breeding values for environmental robustness of viability (i.e., reaction norm slope) and overall viability (reaction norm elevation). These breeding values were regressed against breeding values of viability at two different fluctuating temperatures (with a mean of 25°C or 30°C). Our results based on genetic correlations show that average egg‐to‐adult viability across different constant thermal environments, and not the environmental robustness, was the most important factor for explaining the fitness in fluctuating thermal environments. Our results suggest that the role of environmental robustness in adapting to fluctuating environments might be smaller than anticipated.