Evolutionary history shapes the association between developmental instability and population-level genetic variation in three-spined sticklebacks (original) (raw)

High levels of fluctuating asymmetry in isolated stickleback populations

BMC Evolutionary …, 2012

Background: Fluctuating asymmetry (FA), defined as small random deviations from the ideal bilateral symmetry, has been hypothesized to increase in response to both genetic and environmental stress experienced by a population. We compared levels of FA in 12 bilateral meristic traits (viz. lateral-line system neuromasts and lateral plates), and heterozygosity in 23 microsatellite loci, among four marine (high piscine predation risk) and four pond (zero piscine predation risk) populations of nine-spined sticklebacks (Pungitius pungitius). Results: Pond sticklebacks had on average three times higher levels of FA than marine fish and this difference was highly significant. Heterozygosity in microsatellite markers was on average two times lower in pond (H E % 0.3) than in marine (H E % 0.6) populations, and levels of FA and heterozygosity were negatively correlated across populations. However, after controlling for habitat effect on heterozygosity, levels of FA and heterozygosity were uncorrelated. Conclusions: The fact that levels of FA in traits likely to be important in the context of predator evasion were elevated in ponds compared to marine populations suggests that relaxed selection for homeostasis in ponds lacking predatory fish may be responsible for the observed habitat difference in levels of FA. This inference also aligns with the observation that the levels of genetic variability across the populations did not explain population differences in levels of FA after correcting for habitat effect. Hence, while differences in strength of selection, rather than in the degree of genetic stress could be argued to explain habitat differences in levels of FA, the hypothesis that increased FA in ponds is caused by genetic stress cannot be rejected.

The Genetics and Evolution of Fluctuating Asymmetry

Annual Review of Ecology, Evolution, and Systematics, 2005

■ Abstract Variation in the subtle differences between right and left sides of bilateral characters, or fluctuating asymmetry (FA), has long been considered to be primarily environmental in origin, and this has promoted its use as a measure of developmental instability (DI) in populations. There is little evidence for specific genes that govern FA per se. Numerous studies show that FA levels in various characters are influenced by dominance and especially epistatic interactions among genes. An epistatic genetic basis for FA may complicate its primary use in comparisons of DI levels in outbred or wild populations subjected or not subjected to various environmental stressors. Although the heritability of FA typically is very low or zero, epistasis can generate additive genetic variation for FA that may allow it to evolve especially in populations subjected to bottlenecks, hybridizations, or periods of rapid environmental changes caused by various stresses.

The ontogeny of fluctuating asymmetry

2003

We tested seven hypotheses regarding the mechanisms by which fluctuating asymmetry (FA) originates. We did this by analyzing data on four bilateral characters measured repeatedly during the development of individual domestic fowl. Immediately posthatching, there was substantial directional asymmetry, which rapidly decreased. We detected FA at significant levels in all characters in the majority of our measurements over the remainder of development. We also examined the effects of known environmental stressors (food and density stress) on levels of FA. At the levels we examined, changes in these stressors did not alter the degree of asymmetry we found in fowl. Time series of asymmetry for individuals did not exhibit regular oscillations, as much of the relevant literature predicts. Asymmetry levels reflected the combined effects of developmental noise, which was random in degree and direction, and feedback processes, which decreased asymmetry by altering growth rates on both sides of the body. Our findings best fit the predictions of the residual asymmetry and compensatory growth hypotheses, which suggest that levels of asymmetry reflect only recent growth history.

The Quantitative Genetics of Fluctuating Asymmetry: A Comparison of Two Models

Evolution, 2004

The genetic basis of fluctuating asymmetry (FA), a measure of random deviations from perfect bilateral symmetry, has been the subject of much recent work. In this paper we compare two perspectives on the quantitative genetic analysis of FA and directional asymmetry (DA). We call these two approaches the character-state model and the environmental responsiveness model. In the former approach, the right and left sides are viewed as separate traits whose genetic coupling is manifested by the genetic correlation. This model leads to the relationship,

Why do some traits show higher fluctuating asymmetry than others? A test of hypotheses with tail feathers of birds

Heredity, 2002

Certain characters are more susceptible to increased fluctuating asymmetry (FA) than others. This trait-specific susceptibility has normally been attributed to different degrees of developmental stability, which could be caused by different modes of selection, functionality, or the stress experienced during the development process. Recently, it has also been suggested that the expression of FA not only depends on developmental stability, but also on the cost of growth of the trait, defined as the amount of structural components necessary to form a unit of length of a given character. In accordance with this argument, a trait with more structural components per unit of length should show lower asymmetry than a simpler one. To test this hypothesis, we examine the structure (number of barbs, barb length, and rachis width)

Relating Fluctuating Asymmetries and Mean Values and Discordances of Asymmetries in a Set of Morphological Traits

Symmetry

This study addresses the problem of concordance in fluctuating asymmetry (FA) across traits by analyzing the relationship between FAs and the mean values of character measurements in a set of morphological traits. Regression slopes vary in natural populations, thus, revealing discordance in FA across traits among these populations. Hence, commonly accepted techniques for measuring developmental instability with FA result in uncertainties. Here, I relate FA to mean as a two-dimensional complex to demonstrate the uniformly negative slopes of standardized FA vs. mean value regressions for sets of morphological traits from eighteen distinct natural marine and aquatic populations. Comprehensive analysis of the FA–mean complex cannot be recommended for wide use in assessing stress and fitness, but it offers promise to improve FA measuring methodologies and to better understand the nature of developmental instability.

Fluctuating Asymmetry as an Index of Fitness: Causality or Statistical Artifact?

Oikos, 1999

During the last decade, the study of fluctuating asymmetry (FA) in relation to different fitness aspects has become a popular issue in evolutionary biology. FA is suggested to be important as an index of selective advantage in hoth sexual and natural selection, Evidence for these hypotheses is obtained from field studies in which FA is found to be negatively correlated with various fitness components. In this paper, we demonstrate that the apparent significance of FA may depend on assumptions of linearity between size of a trait and FA, and between trait size and fitness. By means of numerical examples, we show that even small, and probably common, deviations from the assumed linearity can bias the statistical analyses to such an extent that it casts serious doubt on the validity of the postulated causal relationship between FA and fitness. We recommend reanalyses of existing data and emphatically suggest that the underlying statistical assumptions are critically evaluated in future studies of FA, especially concerning linear relationships between the variables.

Heritability of Asymmetry and Lateral Plate Number in the Threespine Stickleback

PLOS One, 2012

The estimation of individual fitness and quality are important elements of evolutionary ecological research. Over the past six decades, there has been great interest in using fluctuating asymmetry (FA) to represent individual quality, yet, serious technical problems have hampered efforts to estimate the heritability of FA, which, in turn, has limited progress in the investigation of FA from an evolutionary