Sexual selection: the importance of long-term fitness measures

New results from a 20-year study of free-living song sparrows confirm that attractive males contribute more offspring than less attractive males. They also reveal that the offspring of preferred males produce more descendents themselves. Females prefer males with a large song repertoire, which further work shows is a condition-dependent indicator of male quality.     

Natural selection on age-specific fertilities in human females: comparison of individual-level fitness measures.

Lifetime reproductive success and timing of reproduction are key components of life-history evolution. To understand the evolution of reproductive schedules, it is important to use a measure of fitness that is sensitive both to reproductive quantity and reproductive timing. There is a contradiction between the theory, which mainly focuses on the rate measures of fitness (r and lambda), and empirical studies, which mainly use lifetime reproductive success (LRS), or some of its correlates, as a fitness measure. We measured phenotypic selection on age-specific fertilities in three pre-modern human populations using individually estimated finite rate of increase, er (lambda). We found that lambda and lifetime reproductive success ranked individuals differently according to their fitness: for example, a female giving birth to four children at a young age may actually have a higher fitness than a female giving birth to six children at a greater age. Increase in fertility at the young age classes (15-19 years) was favoured by selection, but the intensity of selection on fertility was higher in the older age classes (20-30 years), where the variance in fertility was highest. Hence, variation in fertility in the older age classes (20-30) was actually responsible for most of the observed variation in fitness among the individuals. Additionally, more than 90% of variation in fitness (lambda) was attributable to individual differences in LRS, whereas only about 5% of all variation in fitness was due to differences in the reproductive schedule. The rate-sensitive fitness measure did not significantly challenge the importance of total fertility as a component of fitness in humans. However, the rate-sensitive measure clearly allowed more accurate estimation of individual fitness, which may be important for answering some more specific questions.     

Natural selection and the maximization of fitness

The notion that natural selection is a process of fitness maximization gets a bad press in population genetics, yet in other areas of biology the view that organisms behave as if attempting to maximize their fitness remains widespread. Here I critically appraise the prospects for reconciliation. I first distinguish four varieties of fitness maximization. I then examine two recent developments that may appear to vindicate at least one of these varieties. The first is the ‘new’ interpretation of Fisher's fundamental theorem of natural selection, on which the theorem is exactly true for any evolving population that satisfies some minimal assumptions. The second is the Formal Darwinism project, which forges links between gene frequency change and optimal strategy choice. In both cases, I argue that the results fail to establish a biologically significant maximization principle. I conclude that it may be a mistake to look for universal maximization principles justified by theory alone. A more promising approach may be to find maximization principles that apply conditionally and to show that the conditions were satisfied in the evolution of particular traits.     

Variable generation times and Darwinian fitness measures

Summary Reproductive value (RV) and net reproductive output (R _o) are frequently used fitness measures. We argue that they are only appropriate when intervals between reproductive events are fixed, as they are dimensionless generation-to-generation scalings with units offspring per parent. A fitness measure should account for two different effects of a decrease in generation time: (1) increased survival due to shorter exposure to mortality agents and (2) increased frequency of reproduction.R _o andRV deal with the first of these two effects, while a measure with a physical dimensionper time [T^–1] is needed to account for the second. The Malthusian growth parameter,r, meets this requirement and in situations where time to reproduction is variable, we propose, the instantaneous rate of spread of descendants (from an individual) be used instead ofR _o. As an alternative toRV, we suggest using the instantaneous difference = –r, wherer is the population rate of increase. WhileRV andR _o are dimensionless ratios, , and areper time rates which are appropriate in accounting for alterations in generation time.     

The ecology and genetics of fitness in Chlamydomonas. IX. The rate of accumulation of variation of fitness under selection

Populations of Chlamydomonas founded by single cells were cultured in chemostats for 50 days, representing about 125 generations. The mean and variance of division rate was measured daily by withdrawing cells from the effluent and culturing them for 24 h on filtered effluent medium solidified with agar. Mean fitness did not change during the period of culture, and the behavior of neutral markers indicated that no substitutions of novel beneficial mutations occurred. However, the variance of fitness increased markedly at about the same rate in two replicate populations. The standardized rate, or mutational heritability, was Vm/VE = 4-5 x 10(-3) per generation. This is substantially greater than most other estimates for characters closely correlated with fitness. Moreover, it seems difficult to reconcile with the absence of any change in mean fitness. We investigated the possibility that frequency-dependent selection was created by spatial heterogeneity within the culture vessel by testing cell populations with different phenotypes from the top, bottom, and surface of the chemostats. However, the differentiation of these populations seemed to be attributable to phenotypic plasticity, with no evidence that their characteristics were heritable. Finally, we report an experiment in which lines were selected for about 100 generations on solid or liquid medium. These lines became specifically adapted to the medium on which they were cultured, showing that liquid and solid media, even when chemically identical, provide different conditions of growth for Chlamydomonas. The genetic variance appearing in the cultures was therefore attributed to conditionally neutral mutations that were not expressed in the chemostat. This implies that rates of accumulation of mutational variance measured in the culture environment itself (where this can be done) may greatly underestimate the variation available for a response through selection to environmental change. Moreover, it suggests that chemostat populations may be more dynamic and more diverse than is usually thought.     

Direct fitness for dynamic kin selection

The direct-fitness approach to modelling the evolution of social traits is an alternative to the classical inclusive-fitness-based approach. Despite both its utility and popularity, the direct-fitness approach has not yet been extended to include the analysis of dynamic traits, i.e. traits whose level of expression may vary over time. In this article, I apply the direct-fitness approach to cope with the evolution of a dynamic resource-allocation behaviour when this behaviour influences the fitness of relatives. I am able to implement the direct-fitness approach using components (reproductive value, fitness changes and measures of relatedness) found in standard, social-evolutionary models. I illustrate the modified direct-fitness model with an example studied by previous authors, and I show how the direct-fitness perspective can aid the validation of analytical results by means of a genetic algorithm.     

The evolution of altruism: game theory in multilevel selection and inclusive fitness

Although the prisoner's dilemma (PD) has been used extensively to study reciprocal altruism, here we show that the n-player prisoner's dilemma (NPD) is also central to two other prominent theories of the evolution of altruism: inclusive fitness and multilevel selection. An NPD model captures the essential factors for the evolution of altruism directly in its parameters and integrates important aspects of these two theories such as Hamilton's rule, Simpson's paradox, and the Price covariance equation. The model also suggests a simple interpretation of the Price selection decomposition and an alternative decomposition that is symmetrical and complementary to it. In some situations this alternative shows the temporal changes in within- and between-group selection more clearly than the Price equation. In addition, we provide a new perspective on strong vs. weak altruism by identifying their different underlying game structures (based on absolute fitness) and showing how their evolutionary dynamics are nevertheless similar under selection (based on relative fitness). In contrast to conventional wisdom, the model shows that both strong and weak altruism can evolve in periodically formed random groups of non-conditional strategies if groups are multigenerational. An integrative approach based on the NPD helps unify different perspectives on the evolution of altruism.     

The relationship between host selection behaviour and offspring fitness in a koinobiont parasitoid

1. When host quality varies, optimal foraging theory assumes that parasitic wasps select hosts in a manner that increases their individual fitness. In koinobiont parasitoids, where the hosts continue developing for a certain period of time after parasitisation, host selection may not reflect current host quality but may be based on an assessment of future growth rates and resources available for the developing larvae. 2. When presented with hosts of uniform quality, the koinobiont parasitoid Leptomastix dactylopii exhibits a characteristic host‐selection behaviour: some hosts are accepted for oviposition on first encounter, while others are rejected several times before an egg is laid in them, a behaviour that is commonly associated with a changing host acceptance threshold during the course of a foraging bout. 3. The fitness of the offspring that emerged from hosts accepted immediately upon encounter was compared with the fitness of offspring emerged from hosts rejected several times before being accepted for oviposition. 4. The pattern of host acceptance and rejection was not related to any of the measured fitness parameters of the offspring emerging from these hosts (development time, size at emergence, sex ratio at emergence, and female offspring egg load). 5. While complex post facto adaptive explanations can be devised to explain the nature of such a time and energy consuming host selection process, it is suggested that physiological constraints on egg production or oviposition may provide an alternative, purely mechanistic, explanation for the results obtained.     

The shape of selection: using alternative fitness functions to test predictions for selection on flowering time

Selection gradient analysis examines the strength and direction of phenotypic selection as well as the curvature of fitness functions, allowing predictions on and insights into the process of evolution in natural populations. However, traditional linear and quadratic selection analyses are not capable of detecting other features of fitness functions, such as asymmetry or thresholds, which may be relevant for understanding key aspects of selection on many traits. In these cases, additional analyses are needed to test specific hypotheses about fitness functions. In this study we used several approaches to analyze selection on a major life-history trait—flowering time—in the annual plant Brassica rapa subjected to experimentally abbreviated and lengthened growing seasons. We used a model that incorporated a tradeoff between the time allocated to growth versus the time allocated to reproduction in order to predict fitness function shape. The model predicted that optimal flowering time shifts to earlier and later dates as the growing season contracts and expands. It also showed the flowering time fitness function to be asymmetrical: reproductive output increases modestly between the earliest and the optimal flowering date, but then falls sharply with later dates, truncating in a ‘tail of zeros’. Our experimental results strongly supported selection for early flowering in short season and selection for late flowering in long season conditions. We also found support for the predicted asymmetry of the flowering time fitness function, including a ‘tail of zeros’ at later flowering dates. The form of the fitness function revealed here has implications for interpreting estimates of selection on flowering time in natural populations and for refining predictions on evolutionary response to climate change. More generally, this study illustrates the value of diverse statistical approaches to understanding mechanisms of natural selection.     

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.     

Natural selection and fitness entropy in a density-regulated population

The entropy H(p_o,p*) of a population with the initial allele frequency p_o given the equilibrium polymorphic frequency p* has been proposed as a measure of natural selection. In the present paper, we have extended this concept to include a particular aspect of density-dependent selection. We compared size trajectory of a population initially at genetic equilibrium, N(t), with the size trajectories of populations not initially at p*,N(t), but which do eventually converge to a common equilibrium allele frequency and equilibrium density, N*. The following experimentally testable hyopthesis was established. The total area defined by the difference between the trajectories of N(t) and N(t) as they converge to N* is directly proportional to the fitness entropy when population size is transformed using the density-dependent fitness value. Two properties of this relationship were noted. First, it is independent of the magnitude of natural selection and, secondly, it does not depend upon the initial population density as long as the equilibrium and nonequilibrium populations have the same initial numbers. This hypothesis was evaluated with experimental data on the flour beetle Tribolium castaneum.     

Pleiotropy, apparent stabilizing selection and uncovering fitness optima

Evolutionary theory has emphasized that the evolution of single traits cannot be understood in isolation when pleiotropy is present. Widespread pleiotropy causes the appearance of stabilizing selection on metric traits owing to joint effects with fitness, and results in the genetic variation being concentrated in relatively few combinations of the measured traits. In this review, we show how trait combinations with high levels of genetic variation can be used to uncover fitness optima that are defined by apparent stabilizing selection. Defining fitness optima in this way could provide one avenue by which researchers can overcome the problem posed by measuring the myriad of traits that must influence fitness, or by measuring total fitness itself.     

Effects on heterozygosity and reproductive fitness of inbreeding with and without selection on fitness in Drosophila melanogaster

The effects of inbreeding, with (IS) and without selection (IO) for reproductive fitness, on inbreeding depression and heterozygosity were evaluated in 20 lines of each treatment inbred over seven generations using full-sib mating. The survival of lines was significantly greater in IS (20/20) than in IO (15/20). The competitive index measure of reproductive fitness was significantly lower in the inbred lines than in the outbred base population, but not significantly different in surviving IS and IO lines. There was a trend for higher fitness in the IS treatment as relative fitnesses were 19% higher in IS than IO for surviving lines and 59% higher for all lines. Heterozygosities were lower in the inbred lines than in the base population, and significantly higher in the IS than the IO lines. Consequently, the reduction of inbreeding depression in IS has been achieved, at least in part, by slowing the rate of fixation.     

Determinants of male fitness: disentangling intra- and inter-sexual selection

Both intra- and inter-sexual selection may crucially determine a male's fitness. Their interplay, which has rarely been experimentally investigated, determines a male's optimal reproductive strategy and thus is of fundamental importance to the understanding of a male's behaviour. Here we investigated the relative importance of intra- and inter-sexual selection for male fitness in the common lizard. We investigated which male traits predict a male's access to reproduction allowing for both selective pressures and comparing it with a staged mating experiment excluding all types of intra-sexual selection. We found that qualitatively better males were more likely to reproduce and that sexual selection was two times stronger when allowing for both selective pressures, suggesting that inter- and intra-sexual selection determines male fitness and confirming the existence of multi-factorial sexual selection. Consequently, to optimize fitness, males should trade their investment between the traits, which are important for inter- and intra-sexual selection.     

Expected relative fitness and the adaptive topography of fluctuating selection

Wright's adaptive topography describes gene frequency evolution as a maximization of mean fitness in a constant environment. I extended this to a fluctuating environment by unifying theories of stochastic demography and fluctuating selection, assuming small or moderate fluctuations in demographic rates with a stationary distribution, and weak selection among the types. The demography of a large population, composed of haploid genotypes at a single locus or normally distributed phenotypes, can then be approximated as a diffusion process and transformed to produce the dynamics of population size, N, and gene frequency, p, or mean phenotype, . The expected evolution of p or is a product of genetic variability and the gradient of the long-run growth rate of the population, , with respect to p or . This shows that the expected evolution maximizes , the mean Malthusian fitness in the average environment minus half the environmental variance in population growth rate. Thus, as a function of p or represents an adaptive topography that, despite environmental fluctuations, does not change with time. The haploid model is dominated by environmental stochasticity, so the expected maximization is not realized. Different constraints on quantitative genetic variability, and stabilizing selection in the average environment, allow evolution of the mean phenotype to undergo a stochastic maximization of . Although the expected evolution maximizes the long-run growth rate of the population, for a genotype or phenotype the long-run growth rate is not a valid measure of fitness in a fluctuating environment. The haploid and quantitative character models both reveal that the expected relative fitness of a type is its Malthusian fitness in the average environment minus the environmental covariance between its growth rate and that of the population.