Cortland K. Griswold

The evolution of migration in a seasonal environment

Despite the fact that migration occurs in a wide variety of taxa worldwide, little is known about the conditions under which migration is expected to evolve from an ancestral resident population. We develop a model that focuses on ecological factors affecting the evolution of migration in a seasonal environment within a genetically explicit framework. We model the evolution of migration for two common types of migration: ‘shared breeding’ where migrants share a breeding ground with residents and migrate to a separate non-breeding area, versus ‘shared non-breeding’, where migrants share a non-breeding ground with residents and migrate to a separate breeding area. Ecologically, migration is more easily established in the shared-breeding case versus the shared-non-breeding case. Genetically, the additive effect of a migratory allele affects its establishment more in the shared-non-breeding case versus the shared-breeding case, whereas the dominance effect of the allele affects its establishment more in the shared-breeding case versus the shared-non-breeding case. Generally, migratory alleles can invade even when residents are competitively superior to migrants during the shared season. Partial migration occurs when the population is polymorphic for migratory and non-migratory alleles, and is dependent upon which season is shared and the additive and dominance behaviour of the migratory allele.

Carry-over effects, sequential density dependence and the dynamics of populations in a seasonal environment

Most animal populations have distinct breeding and non-breeding periods, yet the implications of seasonality on population dynamics are not well understood. Here, we introduce an experimental model system to study the population dynamics of two important consequences of seasonality: sequential density dependence and carry-over effects (COEs). Using a replicated seasonal population of Drosophila, we placed individuals at four densities in the non-breeding season and then, among those that survived, placed them to breed at three different densities. We show that COEs arising from variation in non-breeding density negatively impacts individual performance by reducing per capita breeding output by 29–77%, implying that non-lethal COEs can have a strong influence on population abundance. We then parametrized a bi-seasonal population model from the experimental results, and show that both sequential density dependence and COEs can stabilize long-term population dynamics and that COEs can reduce population size at low intrinsic rates of growth. Our results have important implications for predicting the successful colonization of new habitats, and for understanding the long-term persistence of seasonal populations in a wide range of taxa, including migratory organisms.

Body size, carry‐over effects and survival in a seasonal environment: consequences for population dynamics

In seasonal populations, vital rates are not only determined by the direct effects of density at the beginning of each season, but also by density at the beginning of past seasons. Such delayed density dependence can arise via non-lethal effects on individuals that carry over to influence per capita rates. In this study, we examine (i) whether parental breeding density influences offspring size, (ii) how this could carry over to affect offspring survival during the subsequent non-breeding period and (iii) the population consequences of this relationship. Using Drosophila melanogaster, the common fruit fly, submitted to distinct breeding and non-breeding seasons, we first used a controlled laboratory experiment to show that high parental breeding density leads to small offspring size, which then affects offspring survival during the non-breeding period but only at high non-breeding densities. We then show that a model with the interaction between parental breeding density and offspring density at the beginning of the non-breeding season best explained offspring survival over 36 replicated generations. Finally, we developed a biseasonal model to show that the positive relationship between parental density and offspring survival can dampen fluctuations in population size between breeding and non-breeding seasons. These results highlight how variation in parental density can lead to differences in offspring quality which result in important non-lethal effects that carry over to influence per capita rates the following season, and demonstrate how this phenomenon can have important implications for the long-term dynamics of seasonal populations.

Density-mediated carry-over effects explain variation in breeding output across time in a seasonal population

In seasonal environments, where density dependence can operate throughout the annual cycle, vital rates are typically considered to be a function of the number of individuals at the beginning of each season. However, variation in density in the previous season could also cause surviving individuals to be in poor physiological condition, which could carry over to influence individual success in the following season. We examine this hypothesis using replicated populations of Drosophila melanogaster, the common fruitfly, over 23 non-overlapping generations with distinct breeding and non-breeding seasons. We found that the density at the beginning of the non-breeding season negatively affected the fresh weight of individuals that survived the non-breeding season and resulted in a 25% decrease in per capita breeding output among those that survived to the next season to breed. At the population level, per capita breeding output was best explained by a model that incorporated density at the beginning of the previous non-breeding season (carry-over effect, COE) and density at the beginning of the breeding season. Our results support the idea that density-mediated COEs are critical for understanding population dynamics in seasonal environments.

A fitness trade-off between seasons causes multigenerational cycles in phenotype and population size

Although seasonality is widespread and can cause fluctuations in the intensity and direction of natural selection, we have little information about the consequences of seasonal fitness trade-offs for population dynamics. Here we exposed populations of Drosophila melanogaster to repeated seasonal changes in resources across 58 generations and used experimental and mathematical approaches to investigate how viability selection on body size in the non-breeding season could affect demography. We show that opposing seasonal episodes of natural selection on body size interacted with both direct and delayed density dependence to cause populations to undergo predictable multigenerational density cycles. Our results provide evidence that seasonality can set the conditions for life-history trade-offs and density dependence, which can, in turn, interact to cause multigenerational population cycles. DOI: http://dx.doi.org/10.7554/eLife.18770.001

The role of seasonality and non-lethal carry-over effects on density-dependent dispersal

Understanding dispersal is critical for predicting a wide range of ecological dynamics. Variation in intraspecific density is widely regarded as a major factor influencing dispersal rates but it is not clear why dispersal is positively related to density in some systems and negatively related to density in other systems. Using seasonal populations of Drosophila melanogaster, we experimentally show that dispersal rates are both positively related to breeding density at the time of dispersal and negatively related to density at the beginning of the previous non-breeding season. This suggests that flies use density at the time of dispersal as a cue for habitat quality but are also negatively influenced by the delayed, non-lethal effects of density in the previous season. A parameterized model indicates that a carry-over effect not only causes a decrease in the proportion of individuals that disperse, but also a decrease in population size caused by lower per capita breeding output. Our results demonstrate how density can have contrasting effects on dispersal and population size depending on when density is measured in the annual cycle and that non-lethal effects on individuals can have important, but previously unrecognized, consequences for both the movement rates and long-term dynamics of seasonal populations.

A comparative study indicates both positive and purifying selection within ryanodine receptor (RyR) genes, as well as correlated evolution

Ryanodine receptors are Ca(2+) ion channels that allow Ca(2+) to flow into the cytosol, from an internal store, in the form of transients. RyRs form a small gene family and vertebrates have three major isoforms, RyR1, RyR2, and RyR3, which are mixed and matched in different combinations in different tissues resulting in different Ca(2+) transients for each tissue. In this study, we characterized the interspecies evolution of RyRs within vertebrates. First, we compared the nucleotide divergence of key gene regions including divergent regions (DRs), which are believed to be responsible for the functional divergence between RyRs, and mutation hot-spot regions, which are responsible for RyR-related pathologies. We found evidence that DRs undergo positive selection and mutation hot-spot regions undergo purifying selection. Second, we estimated the extent of purifying selection for RyR1, RyR2, and RyR3 by estimating dN/dS ratios. We found all three genes to be under strong purifying selection, overall. This is consistent with RyRs being used in a diverse set of physiological contexts and therefore under potentially high pleiotropic constraint. Third, we tested for the correlated evolution of dN/dS ratios between RyR genes. We found that RyR2 and RyR3, and RyR3 and a skeletal form of dihydropyridine receptor (DHPR) have correlated rates of evolution. We propose that compensatory effects may explain their correlated evolution. We tested for compensatory function by simulating mutations via a physiological model of RyR function, but did not find evidence for compensation, which indicates that the correlation is likely a result of another process.

Epistasis can increase multivariate trait diversity in haploid non-recombining populations

We evaluate the effect of epistasis on genetically-based multivariate trait variation in haploid non-recombining populations. In a univariate setting, past work has shown that epistasis reduces genetic variance (additive plus epistatic) in a population experiencing stabilizing selection. Here we show that in a multivariate setting, epistasis also reduces total genetic variation across the entire multivariate trait in a population experiencing stabilizing selection. But, we also show that the pattern of variation across the multivariate trait can be more even when epistasis occurs compared to when epistasis is absent, such that some character combinations will have more genetic variance when epistasis occurs compared to when epistasis is absent. In fact, a measure of generalized multivariate trait variation can be increased by epistasis under weak to moderate stabilizing selection conditions, as well as neutral conditions. Likewise, a measure of conditional evolvability can be increased by epistasis under weak to moderate stabilizing selection and neutral conditions. We investigate the nature of epistasis assuming a multivariate-normal model genetic effects and investigate the nature of epistasis underlying the biophysical properties of RNA. Increased multivariate diversity occurs for populations that are infinite in size, as well as populations that are finite in size. Our model of finite populations is explicitly genealogical and we link our findings about the evenness of eigenvalues with epistasis to prior work on the genealogical mapping of epistatic effects.

The mapping of epistatic effects onto a genealogical tree in haploid populations.

In this paper we present a model that maps epistatic effects onto a genealogical tree for a haploid population. Prior work has demonstrated that genealogical structure causes the genotypic values of individuals to covary. Our results indicate that epistasis can reduce genotypic covariance that is caused by genealogical structure. Genotypic effects (both additive and epistatic) occur along the branches of a genealogical tree, from the base of the tree to its tips. Epistasis reduces genotypic covariance because there is a reweighting of the contribution of branches to the states of genotypes compared to the additive case. Branches near the tips of a genealogical tree contribute proportionally more genetic effects with epistasis than without epistasis. Epistatic effects are most numerous at basal positions in a genealogical tree when a population is constant in size and experiencing no selection, optimizing selection, diversifying selection or directional selection, indicating that epistatic effects are typically old. For a population that is growing in size, epistatic effects are most numerous at midpoints in a genealogical tree, indicating epistatic effects are of moderate age. Our results are important in that they suggest epistatic effects may typically explain deep (old) divergences and broad patterns of divergence that exist in populations, except in growing populations. In a growing population, epistatic effects may cause more within group divergence higher up in a tree and less between group divergence that is deep in a tree. The distribution of the number of epistatic effects and the expected variance and covariance in the number of epistatic effects is also provided assuming neutrality.

Epistasis can accelerate adaptive diversification in haploid asexual populations

A fundamental goal of the biological sciences is to determine processes that facilitate the evolution of diversity. These processes can be separated into ecological, physiological, developmental and genetic. An ecological process that facilitates diversification is frequency-dependent selection caused by competition. Models of frequency-dependent adaptive diversification have generally assumed a genetic basis of phenotype that is non-epistatic. Here, we present a model that indicates diversification is accelerated by an epistatic basis of phenotype in combination with a competition model that invokes frequency-dependent selection. Our model makes use of a genealogical model of epistasis and insights into the effects of balancing selection on the genealogical structure of a population to understand how epistasis can facilitate diversification. The finding that epistasis facilitates diversification may be informative with respect to empirical results that indicate an epistatic basis of phenotype in experimental bacterial populations that experienced adaptive diversification.