What explains rare and conspicuous colours in a snail? A test of time-series data against models of drift, migration or selection

K Johannesson,R K Butlin

doi:10.1038/hdy.2016.77

Abstract

It is intriguing that conspicuous colour morphs of a prey species may be maintained at low frequencies alongside cryptic morphs. Negative frequency-dependent selection by predators using search images (‘apostatic selection’) is often suggested without rejecting alternative explanations. Using a maximum likelihood approach we fitted predictions from models of genetic drift, migration, constant selection, heterozygote advantage or negative frequency-dependent selection to time-series data of colour frequencies in isolated populations of a marine snail (Littorina saxatilis), re-established with perturbed colour morph frequencies and followed for >20 generations. Snails of conspicuous colours (white, red, banded) are naturally rare in the study area (usually <10%) but frequencies were manipulated to levels of ~50% (one colour per population) in 8 populations at the start of the experiment in 1992. In 2013, frequencies had declined to ~15–45%. Drift alone could not explain these changes. Migration could not be rejected in any population, but required rates much higher than those recorded. Directional selection was rejected in three populations in favour of balancing selection. Heterozygote advantage and negative frequency-dependent selection could not be distinguished statistically, although overall the results favoured the latter. Populations varied idiosyncratically as mild or variable colour selection (3–11%) interacted with demographic stochasticity, and the overall conclusion was that multiple mechanisms may contribute to maintaining the polymorphisms.

Highlights

In finite populations, genetic variation is reduced through the combined effects of drift and selection
Many of natural populations are likely to be far from equilibrium and unstable polymorphisms may be sustained over extended periods of time owing to stochastic effects during colonization, range expansion and population perturbation (Cook, 1998; Excoffier et al, 2009)
Overall, we observed that the frequencies of the different conspicuous colour morphs declined over the time period of observations (21 years)

Summary

Introduction

Genetic variation is reduced through the combined effects of drift and selection. Populations of many species are polymorphic for inherited traits that are likely to affect individual fitness, such as colour. Even in well-studied species and over short evolutionary timescales, it is often challenging to explain how colour polymorphisms are maintained (see, for example, Clarke, 1962; Cook, 1998, 2007; Cook and Saccheri, 2013; McLean and Stuart-Fox, 2014). If colour does not affect fitness, or is under weak selection, a polymorphism will be more or less structured in time and space by gene flow, population demography and history. Many (perhaps the majority) of natural populations are likely to be far from equilibrium and unstable polymorphisms may be sustained over extended periods of time owing to stochastic effects during colonization, range expansion and population perturbation (Cook, 1998; Excoffier et al, 2009). Selection should only be invoked with caution when seeking to explain colour polymorphism

Methods

Results

Conclusion