Demographic constraints in evolution: Towards unifying the evolutionary theories of senescence and niche conservatism

Summary I suggest that there may be a fundamental conceptual unity between two seemingly disparate phenomena: (1) senescence (the progressive deterioration in physiological function and, thus, individual fitness with age) and (2) niche conservatism (the observation that species often seem rather fixed over evolutionary time in their basic niche properties). I argue that both phenomena arise from demographic asymmetries. The evolutionary theory of ageing rests on the observation that the force of selection declines with age, reflecting the basic demographic facts that in persistent populations there are always fewer individuals in old than in young age classes and these individuals tend to have lower reproductive value. A similar demographic asymmetry arises when populations inhabit environments with source habitats (i.e. where conditions are within the species' niche) and sink habitats (where conditions lie outside the niche): there tend to be more individuals in sources than in sinks and individuals in sources have relatively higher reproductive values. These demographic asymmetries should often imply that the force of selection is greater in sources than in sinks, leading automatically towards niche conservatism. I suggest that niche evolution is most likely in circumstances where these demographic asymmetries in space weaken or reverse.     

Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution

Species interactions commonly coevolve as complex geographic mosaics of populations shaped by differences in local selection and gene flow. We use a haploid matching-alleles model for coevolution to evaluate how a pair of species coevolves when fitness interactions are reciprocal in some locations ("hot spots") but not in others ("cold spots"). Our analyses consider mutualistic and antagonistic interspecific interactions and a variety of gene flow patterns between hot and cold spots. We found that hot and cold spots together with gene flow influence coevolutionary dynamics in four important ways. First, hot spots need not be ubiquitous to have a global influence on evolution, although rare hot spots will not have a disproportionate impact unless selection is relatively strong there. Second, asymmetries in gene flow can influence local adaptation, sometimes creating stable equilibria at which species experience minimal fitness in hot spots and maximal fitness in cold spots, or vice versa. Third, asymmetries in gene flow are no more important than asymmetries in population regulation for determining the maintenance of local polymorphisms through coevolution. Fourth, intraspecific allele frequency differences among hot and cold spot populations evolve under some, but not all, conditions. That is, selection mosaics are indeed capable of producing spatially variable coevolutionary outcomes across the landscapes over which species interact. Altogether, our analyses indicate that coevolutionary trajectories can be strongly shaped by the geographic distribution of coevolutionary hot and cold spots, and by the pattern of gene flow among populations.     

Limits to length asymmetry detection in starlings: implications for biological signalling

Fluctuating asymmetry has received considerable recent attention in evolutionary biology as these small developmental asymmetries can be related to biological fitness and, hence, could be used as a visual cue (or signal) of quality among individuals. The ability of signal receivers to detect and respond to small asymmetries is a fundamental assumption of the symmetry-signalling hypothesis, but has not been experimentally investigated. In this study I have investigated the perceptual threshold to detect and respond to paired-bar length asymmetry in a common bird, the European starling Sturnus vulgaris, by means of operant-learning techniques. The threshold indicates how large the length asymmetry must be to be reliably discriminated from symmetry; birds could not detect an asymmetry of 1.25%. In nature, many asymmetries can be smaller than 1.25%, hence this initial study suggests that caution should be used when trying to invoke symmetry-signalling in natural populations.     

Strategic mating with common preferences

We present a two-sided search model in which individuals from two groups (males and females, employers and workers) would like to form a long-term relationship with a highly ranked individual of the other group, but are limited to individuals who they randomly encounter and to those who also accept them. This article extends the research program, begun in Alpern and Reyniers [1999. J. Theor. Biol. 198, 71-88], of providing a game theoretic analysis for the Kalick-Hamilton [1986. J. Personality Soc. Psychol. 51, 673-682] mating model in which a cohort of males and females of various 'fitness' or 'attractiveness' levels are randomly paired in successive periods and mate if they accept each other. Their model compared two acceptance rules chosen to represent homotypic (similarity) preferences and common (or 'type') preferences. Our earlier paper modeled the first kind by assuming that if a level x male mates with a level y female, both get utility -|x-y|, whereas this paper models the second kind by giving the male utility y and the female utility x. Our model can also be seen as a continuous generalization of the discrete fitness-level game of Johnstone [1997. Behav. Ecol. Sociobiol. 40, 51-59]. We establish the existence of equilibrium strategy pairs, give examples of multiple equilibria, and conditions guaranteeing uniqueness. In all equilibria individuals become less choosy over time, with high fitness individuals pairing off with each other first, leaving the rest to pair off later. This route to assortative mating was suggested by Parker [1983. Mate Choice, Cambridge University Press, Cambridge, pp. 141-164]. If the initial fitness distributions have atoms, then mixed strategy equilibria may also occur. If these distributions are unknown, there are equilibria in which only individuals in the same fitness band are mated, as in the steady-state model of MacNamara and Collins [1990. J. Appl. Prob. 28, 815-827] for the job search problem.     

Ideal free distributions when individuals differ in competitive ability: phenotype-limited ideal free models

A series of prospective models is developed to investigate ideal free distributions in populations where individuals differ in competitive ability. The models are of three types. In the continuous-input models, there is continuous arrival of food or mates into each habitat patch, and competitors scramble to obtain as large a share as possible. In the interference models, the prey density in a particular patch stays constant but the presence of competitors slows down the rate at which prey are captured. In the kleptoparasitism model, individuals have food or females stolen from them by competitors higher in the dominance hierarchy, and in turn steal items from subordinates. A general result of the continuous-input and interference models is that the population of competitors can be truncated between patches so that the individuals with the highest competitive ability occur in the best patches, or in the patches where competitive differences are greatest. Individuals of lowest competitive ability occur in the poorest patches or where competitive differences are least, and intermediate phenotypes are ranked between these two extremes. Thus the ideal free prediction that all individuals will achieve equal fitness will not apply. However, in continuous-input cases where competitive differences between phenotypes remain constant across patches, this solution is only neutrally stable, and forms only one element of a set of equilibrium distributions. The fact that many empirical studies of continuous-input have found approximately equal mean fitness across patches may relate to this finding. Most interference studies contradict the simple ideal free solution by having different mean intake rates across patches; this may relate to the predicted positive correlation of competitive ability with patch quality. The kleptoparasitism model usually generated continuous cycling of individuals between habitat patches, though some correlation could be found between competitive ability and patch quality.     

Negative Correlation between Ant and Spider Abundances in the Canopy of a Bornean Tropical Rain Forest

In tropical rain forests, high canopy trees have diverse and abundant populations of ants and spiders. However, accessing high trees and their fauna remains difficult; thus, how ants and spiders interact in the canopy remains unclear. To better understand the interspecific interactions between these two dominant arthropod groups, we investigated their spatial distributions at the canopy surface in a tropical rain forest in Borneo. We sampled ants and spiders six times between 2009 and 2011 by sweeping with an insect net at the tree crown surfaces of 190 emergent or tall (≥20 m in height) trees. We collected 438 ant individuals belonging to 94 species and 1850 spider individuals (1630 juveniles and 220 adults) belonging to 142 morphospecies (adults only) from a total of 976 samples. The fact that we collected four times more spider individuals than ant individuals suggests that fewer ants forage at the tree crown surface than previously thought. The number of spider individuals negatively correlated with the number of ant individuals and the number of ant species, indicating significant exclusivity between ant and spider spatial distributions at the tree crown surface. Niche‐overlap between the two taxa confirmed this observation. Although our data do not address the causes of these spatial distributions, antagonistic interspecific interactions such as interference behaviors and intra‐guild predation are ecological mechanisms that give rise to exclusive spatial distributions.     

Kin selection in age-structured populations

There have been several discussions in the literature as to how to weight interactions between individuals of different ages in models of kin selection. It has commonly been assumed that the reproductive value of a given age is the most appropriate weight, for the purpose of calculating its contribution to inclusive fitness. This paper analyses a model of kin selection in an age-structured population. It is shown that reproductive value is relevant to behavioural interactions involving effects on survival, although the reproductive value of a given age does not provide an exact weighting of its fitness contribution in either discrete- or continuous-time populations. Reproductive value is not relevant to interactions involving effects on fecundity. The results are discussed in relation to observations on behavioural asymmetries involving age differences.     

Fitness costs in spatially structured environments

The clustering of individuals that results from limited dispersal is a double‐edged sword: although it allows for local interactions to be mostly among related individuals, it also results in increased local competition. Here I show that, because they mitigate local competition, fitness costs such as reduced fecundity or reduced survival are less costly in spatially structured environments than in nonspatial settings. I first present a simple demographic example to illustrate how spatial structure weakens selection against fitness costs. Then, I illustrate the importance of disentangling the evolution of a trait from the evolution of potential associated costs, using an example taken from a recent study investigating the effect of spatial structure on the evolution of host defense. In this example indeed, the differences between spatial and nonspatial selection gradients are due to differences in the fitness costs, thereby undermining interpretations of the results made in terms of the trait only. This illustrates the need to consider fitness costs as proper traits in both theoretical and empirical studies.     

Evolution of fitnesses and allele frequencies in a population with spatially heterogeneous selection pressures

The level of gene flow considerably influences the outcome of evolutionary processes in structured populations with spatial heterogeneity in selection pressures; low levels of gene flow may allow local adaptation whereas high levels of gene flow may oppose this process thus preventing the stable maintenance of polymorphism. Indeed, proportions of fitness space that successfully maintain polymorphism are substantially larger in spatially heterogenous populations with lower to moderate levels of gene flow when compared to single-deme models. Nevertheless, the effect of spatial heterogeneity on the evolutionary construction of polymorphism is less clear. We have investigated the levels of polymorphism resulting from a simple two-deme construction model, which incorporates recurrent mutation as well as selection. We further compared fitness properties, stability of equilibria, and frequency distribution patterns emerging from the construction approach and compared these to the static fitness-space approach. The construction model either promotes or constrains the level of polymorphisms, depending on the levels of gene flow. Comparison of the fitness properties resulting from both approaches shows that they maintain variation in different parts of fitness space. The part of fitness space resulting from construction is more stable than that implied by the ahistoric fitness-space approach. Finally, the equilibrium allele-frequency distribution patterns vary substantially with different levels of gene flow, underlining the importance of correctly sampling spatial structure if these patterns are to be used to estimate population-genetic processes.     

Evolutionary Stability for Interactions among Kin under Quantitative Inheritance

The theory of evolutionarily stable strategies (ESS) predicts the long-term evolutionary outcome of frequency-dependent selection by making a number of simplifying assumptions about the genetic basis of inheritance. I use a symmetrized multilocus model of quantitative inheritance without mutation to analyze the results of interactions between pairs of related individuals and compare the equilibria to those found by ESS analysis. It is assumed that the fitness changes due to interactions can be approximated by the exponential of a quadratic surface. The major results are the following. (1) The evolutionarily stable phenotypes found by ESS analysis are always equilibria of the model studied here. (2) When relatives interact, one of the two conditions for stability of equilibria differs between the two models; this can be accounted for by positing that the inclusive fitness function for quantitative characters is slightly different from the inclusive fitness function for characters determined by a single locus. (3) The inclusion of environmental variance will in general change the equilibrium phenotype, but the equilibria of ESS analysis are changed to the same extent by environmental variance. (4) A class of genetically polymorphic equilibria occur, which in the present model are always unstable. These results expand the range of conditions under which one can validly predict the evolution of pairwise interactions using ESS analysis.     

The ecology of asymmetry in stickleback defense structures

Slight departures from bilateral symmetry are usually associated with reduced fitness. Here we show that an insular freshwater population of Gasterosteus aculeatus exhibits spatial and temporal segregation according to the incidence and direction of asymmetry in the number of bony lateral plates, which are important predator-defense structures. We analyzed 11,263 fish collected from 19 full lake transects over three years, and found that signed asymmetries for plate number were slightly left-side biased. Asymmetries occurred in 55% of the stickleback with more asymmetrics found during cold weather, and more left-biased individuals found during windy conditions, possibly due to environmentally driven activity levels that differ among asymmetric forms. Absolute plate asymmetries were randomly distributed in the lake, but there was a strong shift in signed plate asymmetry from a mean of zero in littoral zones to left-side bias in limnetic zones, probably due to microhabitat choices among asymmetric forms. Video data of avian piscivores on the lake show laterality in prey handling, providing a potential mechanism for asymmetric prey morphology. Our results imply a complex relationship between slight asymmetries and niche space that is relevant to the broader literature on the evolutionary implications of developmental instability and intrapopulation variability.     

Ideal free distributions, evolutionary games, and population dynamics in multiple-species environments

In this article, we develop population game theory, a theory that combines the dynamics of animal behavior with population dynamics. In particular, we study interaction and distribution of two species in a two-patch environment assuming that individuals behave adaptively (i.e., they maximize Darwinian fitness). Either the two species are competing for resources or they are in a predator-prey relationship. Using some recent advances in evolutionary game theory, we extend the classical ideal free distribution (IFD) concept for single species to two interacting species. We study population dynamical consequences of two-species IFD by comparing two systems: one where individuals cannot migrate between habitats and one where migration is possible. For single species, predator-prey interactions, and competing species, we show that these two types of behavior lead to the same population equilibria and corresponding species spatial distributions, provided interspecific competition is patch independent. However, if differences between patches are such that competition is patch dependent, then our predictions strongly depend on whether animals can migrate or not. In particular, we show that when species are settled at their equilibrium population densities in both habitats in the environment where migration between habitats is blocked, then the corresponding species spatial distribution need not be an IFD. Thus, when species are given the opportunity to migrate, they will redistribute to reach an IFD (e.g., under which the two species can completely segregate), and this redistribution will also influence species population equilibrial densities. Alternatively, we also show that when two species are distributed according to the IFD, the corresponding population equilibrium can be unstable.     

Density dependence forces divergent population growth rates and alters occupancy patterns of a central place foraging Antarctic seabird

Density‐dependent regulation is an important process in spatio‐temporal population dynamics because it can alter the effects of synchronizing processes operating over large spatial scales. Most frequently, populations are regulated by density dependence when higher density leads to reduced individual fitness and population growth, but inverse density dependence can also occur when small populations are subject to higher extinction risks. We investigate whether density‐dependent regulation influences population growth for the Antarctic breeding Adélie penguin Pygoscelis adeliae. Understanding the prevalence and nature of density dependence for this species is important because it is considered a sentinel species reflecting the impacts of fisheries and environmental change over large spatial scales in the Southern Ocean, but the presence of density dependence could introduce uncertainty in this role. Using data on population growth and indices of resource availability for seven regional Adélie penguin populations located along the East Antarctic coastline, we find compelling evidence that population growth is constrained at some locations by the amount of breeding habitat available to individuals. Locations with low breeding habitat availability had reduced population growth rates, higher overall occupancy rates, and higher occupancy of steeper slopes that are sparsely occupied or avoided at other locations. Our results are consistent with evolutionary models of avian breeding habitat selection where individuals search for high‐quality nest sites to maximize fitness returns and subsequently occupy poorer habitat as population density increases. Alternate explanations invoking competition for food were not supported by the available evidence, but strong conclusions on food‐related density dependence were constrained by the paucity of food availability data over the large spatial scales of this region. Our study highlights the importance of incorporating nonconstant conditions of species–environment relationships into predictive models of species distributions and population dynamics, and provides guidance for improved monitoring of fisheries and climate change impacts in the Southern Ocean.     

Mating system contributes only slightly to female maintenance in gynodioecious Geranium maculatum (Geraniaceae)

Gynodioecy, the co-occurrence of female and hermaphroditic individuals within a population, is an important intermediate in the evolution of separate sexes. The first step, female maintenance, requires females to have higher seed fitness compared with hermaphrodites. A common mechanism thought to increase relative female fitness is inbreeding depression avoidance, the magnitude of which depends on hermaphroditic selfing rates and the strength of inbreeding depression. Less well studied is the effect of biparental inbreeding on female fitness. Biparental inbreeding can affect relative female fitness only if its consequence or frequency differs between sexes, which could occur if sex structure and genetic structure both occur within populations. To determine whether inbreeding avoidance and/or biparental inbreeding can account for female persistence in Geranium maculatum, we measured selfing and biparental inbreeding rates in four populations and the spatial genetic structure in six populations. Selfing rates of hermaphrodites were low and did not differ significantly from zero in any population, leading to females gaining at most a 1–14% increase in seed fitness from inbreeding avoidance. Additionally, although significant spatial genetic structure was found in all populations, biparental inbreeding rates were low and only differed between sexes in one population, thereby having little influence on female fitness. A review of the literature revealed few sexual differences in biparental inbreeding among other gynodioecious species. Our results show that mating system differences may not fully account for female maintenance in this species, suggesting other mechanisms may be involved.     

Disturbance-dependent spatial distribution of sexes in a gynodioecious understory shrub

Several ecological conditions and processes occurring naturally in plant populations may lead to spatial aggregation of sexes within populations of sexually polymorphic species. In addition, ecological disturbances such as forest management or fire could also affect the spatial distribution of sexes within populations. Spatial aggregation of sexes can have important consequences for the fitness of the individuals in sex-biased patches through increased pollen limitation and/or variation in the male fitness of hermaphrodites. Therefore, spatial aggregation of sexes could be relevant for the maintenance of the sexual polymorphism in plant species. Here, we used point pattern analysis to study the spatial distribution of female and hermaphrodite individuals within a single population of the gynodioecious understory shrub Daphne laureola, inhabiting a young pine reforestation and the adjacent natural undisturbed area. In the undisturbed area, we found that hermaphrodites were distributed randomly whereas females were spatially aggregated at short distances. Such aggregation could result from narrower ecological amplitude, cyto-nuclear determination of sex and limited dispersal and/or increased cloning in females. In the reforested area, females were slightly more abundant and the two sexes were randomly distributed among all plants. Recolonization processes after certain forest disturbances could thus favour the establishment of females and alter the spatial distribution of sexes in this understory species.     

The significance of over- and underdominance for the maintenance of genetic polymorphisms. II. Overdominance and instability with random mating

Part I of the present series demonstrates that globally stable polymorphic equilibria may show underdominance in Darwinian fitness. Hence, overdominance in fitness can no longer be conceived of as a necessary condition for the stability of a polymorphism. In the present paper, the question is posed as to whether overdominance is at least sufficient for this stability. A population of randomly mating individuals is considered, where selection operates uniquely through differential fecundities of particular mating types and may generate either a heterozygote excess or deficit relative to Hardy-Weinberg proportions. It turns out that both unstable central overdominance and stable central underdominance are possible and that their occurrence is strongly related to an excess or a deficiency of heterozygotes in the vicinity of the regions of instability or stability. As one consequence, the above suggested sufficiency of heterozygote superiority is not valid, even in random mating populations. Based on the results of both papers of this series, which demonstrate the inadequacy of over- and underdominance as indicators of stability or instability, a modified overdominance principle is discussed. This principle states that a biallelic polymorphism is maintained if the heterozygote is superior in its degree of "heterogamous self-replication" to the degrees of "autogamous self-replication" of the corresponding homozygotes. It is derived with the help of fractional fitnesses, and it is pointed out that certain ratios of these may be more useful for finding evolutionary constants which govern the maintenance of genetic polymorphisms than are ratios of total fitnesses.     

Spatial Segregation of the Sexes and Nutrients affect Reproductive Success in a Dioecious Wind-pollinated Grass

In many dioecious plant species in which spatial distributions of males and females have been examined, the sexes are spatially segregated – usually along an environmental gradient. Unless pollen is uniformly distributed in a population, spatial segregation of the sexes should reduce the average mating success of individuals. In three Californian populations of Distichlis spicata – a wind-pollinated grass species that exhibits spatial segregation of the sexes – I examined patterns of pollen movement and the effects of pollen load and nutrient availability on seed set to determine whether spatial segregation of the sexes actually reduces mating success for both males and females. In two of the populations, pollen dispersal was restricted, and pollen augmentation consistently, significantly increased seed set. However, in the third population – which had the lowest seed set – I found that although there were some indications of pollen limitation, pollen dispersal was not restricted, and seed production was limited primarily by nutrient availability. These results imply that in some populations of D. spicata nutrient limitation on the production of seeds by females may be sufficiently strong that spatial segregation of the sexes causes a fairly low cost to reproductive success compared with a more random distribution of the sexes. However, in other populations, pollen does limit mating success, and the spatial segregation of males and females in these populations is reducing the fecundity of both males and females.     

Evolutionary genomics of host adaptation in vesicular stomatitis virus

Populations experiencing similar selection pressures can sometimes diverge in the genetic architectures underlying evolved complex traits. We used RNA virus populations of large size and high mutation rate to study the impact of historical environment on genome evolution, thus increasing our ability to detect repeatable patterns in the evolution of genetic architecture. Experimental vesicular stomatitis virus populations were evolved on HeLa cells, on MDCK cells, or on alternating hosts. Turner and Elena (2000. Cost of host radiation in an RNA virus. Genetics. 156:1465-1470.) previously showed that virus populations evolved in single-host environments achieved high fitness on their selected hosts but failed to increase in fitness relative to their ancestor on the unselected host and that alternating-host-evolved populations had high fitness on both hosts. Here we determined the complete consensus sequence for each evolved population after 95 generations to gauge whether the parallel phenotypic changes were associated with parallel genomic changes. We also analyzed the patterns of allele substitutions to discern whether differences in fitness across hosts arose through true pleiotropy or the presence of not only a mutation that is beneficial in both hosts but also 1 or more mutations at other loci that are costly in the unselected environment (mutation accumulation [MA]). We found that ecological history may influence to what extent pleiotropy and MA contribute to fitness asymmetries across environments. We discuss the degree to which current genetic architecture is expected to constrain future evolution of complex traits, such as host use by RNA viruses.     

Genetic structure of age classes in Camellia japonica (Theaceae)

Camellia japonica L. (Theaceae), an insect- and bird-pollinated, broad-leaved evergreen tree, is widely distributed in Japan and the southern Korean peninsula. The species has a relatively even age distribution within populations, which may influence the spatial genetic structure of different age classes relative to species with typical L-shaped age distributions. To determine whether the internal spatial genetic structure found in seedlings and young individuals carries over into adults, we used allozyme loci, F-statistics, spatial autocorrelation statistics (Moran's I), and coancestry measures to examine changes in genetic structure among seven age classes in a population (60-m x 100-m area) in southern Korea. In seedlings, weak but significant positive values of Moran's I-statistics and coancestry measures were found for distances less than 14 m, which is consistent with a mechanism of limited seed dispersal combined with overlapping seed shadows. This spatial structure, however, dissipates in older age classes, and in adults genetic variation has an essentially random spatial distribution. Morisita's index of dispersion of individuals in each age class showed that seedlings and juveniles are more highly clustered than are older individuals. These results suggest that self-thinning changes the spatial relationships of individuals, and thus genotypes. A multilocus estimate of FST (0.008) shows a small but statistically significant difference in allele frequencies among age classes. In summary, intrapopulation genetic structure within and among age classes of C. japonica was significant but weak. Despite presumably limited seed dispersal, weak spatial genetic structure in juveniles suggests overlapping seed shadows followed by self-thinning during recruitment. The present study also demonstrates that studies of spatial genetic structure focusing on limited numbers of generations may not be sufficient to reveal the entire picture of genetic structure in populations with overlapping generations.     

Plastic reproductive strategies in a clonal marine invertebrate

Plastic reproductive allocation may allow individuals to maximize their fitness when conditions vary. Mate availability is one condition that may determine the fitness of an individual's allocation strategy. Using a variety of methods, I detected evidence of plastic allocation to asexual (clonal) reproduction in response to mate availability in the brittle star Ophiactis savignyi. There were more mature individuals in populations in which both sexes were present, and clones from these populations had fewer clone-mates than clones from single-sex populations. Animals placed with mates in a field experiment divided less frequently than animals without a mate. These findings demonstrate that animals reduce their allocation to asexual reproduction when mates are present and when a loss of fecundity associated with cloning would decrease offspring production. This plasticity is probably adaptive because it maximizes sexual-reproductive potential when fertilization is more likely, but maximizes survival of the clone when mates are absent and gametes are unlikely to be converted to offspring.