The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species

Bolton, Peri E.; Rollins, Lee A.; Griffith, Simon C.

doi:10.1111/mec.13201

Cited by 28 publications

(64 citation statements)

References 132 publications

(146 reference statements)

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“…Another recent source of discussion and controversy is the consequence of colour polymorphisms on various aspects of population performance or population fitness, such as extinction risk, productivity or geographical range (Bolton et al . , ; Forsman ). Forsman () cites several experimental studies from his own research laboratory in support of his hypothesis that polymorphic populations or species have higher viability and/or lower extinction risk.…”

Section: Correlational Selection and The Origin Of Multiple Trait Difmentioning

confidence: 99%

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Back to basics: using colour polymorphisms to study evolutionary processes

Svensson

2017

Molecular Ecology

104

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Here, I suggest that colour polymorphic study systems have been underutilized to answer general questions about evolutionary processes, such as morph frequency dynamics between generations and population divergence in morph frequencies. Colour polymorphisms can be used to study fundamental evolutionary processes like frequency-dependent selection, gene flow, recombination and correlational selection for adaptive character combinations. However, many previous studies of colour polymorphism often suffer from weak connections to population genetic theory. I argue that too much focus has been directed towards noticeable visual traits (colour) at the expense of understanding the evolutionary processes shaping genetic variation and covariation associated with polymorphisms in general. There is thus no need for a specific evolutionary theory for colour polymorphisms beyond the general theory of the maintenance of polymorphisms in spatially or temporally variable environments or through positive or negative frequencydependent selection. I outline an integrative research programme incorporating these processes and suggest some fruitful avenues in future investigations of colour polymorphisms.

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Section: Correlational Selection and The Origin Of Multiple Trait Difmentioning

confidence: 99%

“…,b; McKinnon & Pierotti ), and this increasing interest is illustrated by a recent review in Molecular Ecology (Bolton et al . ) that spurred some disagreement and a recent discussion (Bolton et al . ; Forsman ).…”

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confidence: 99%

Back to basics: using colour polymorphisms to study evolutionary processes

Svensson

2017

Molecular Ecology

104

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“…Bolton et al . () state that a clearer distinction should be made between geographic polymorphisms and ‘true polymorphic species’ and argue that the beneficial effects of polymorphism are less likely to apply in sympatric polymorphic systems. In response, I question the definition of ‘true polymorphic species’ sensu Bolton et al .…”

Section: On Historical Definitions and The Importance Of Recognizing mentioning

confidence: 99%

“…In response, I question the definition of ‘true polymorphic species’ sensu Bolton et al . (), as species showing both morphs co‐occurring across the entire range of a species and as being generally distinct from species that have clinal or allopatric variation in phenotype (Fig. a and b in Bolton et al .…”

Section: On Historical Definitions and The Importance Of Recognizing mentioning

confidence: 99%

Is colour polymorphism advantageous to populations and species?

Forsman

2016

Molecular Ecology

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I am writing in response to an article by Bolton, Rollins and Griffith (2015) entitled 'The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species' that was recently published as an Opinion under the NEWS AND VIEWS section in Molecular Ecology. Bolton et al. (Molecular Ecology, 2015, 24, 2907 argue that colour polymorphism may reduce population fitness and increase extinction risk and emphasize that this is contrary to predictions put forward by Forsman et al. (Ecology, 89, 2008, 34) and Wennersten & Forsman (Biological Reviews 87, 2012, 756) that the existence of multiple colour morphs with co-adapted gene complexes and associated trait values may increase the ecological and evolutionary success of polymorphic populations and species. Bolton et al. (Molecular Ecology, 2015, 24, 2907 further state that there is no clear evidence from studies of 'true polymorphic species' that polymorphism promotes population persistence. In response, I (i) challenge their classifications of polymorphisms and revisit the traditional definitions recognizing the dynamic nature of polymorphisms, (ii) review empirical studies that have examined whether and how polymorphism is associated with extinction risk, (iii) discuss the roles of trait correlations between colour pattern and other phenotypic dimensions for population fitness and (iv) highlight that the causes and mechanisms that influence the composition and maintenance of polymorphisms are different from the consequences of the polymorphic condition and how it may impact on aspects of ecological success and long-term persistence of populations and species.Keywords: colour polymorphisms, evolution, extinction risk, geographic variation, population persistence, speciation History of research on adaptive polymorphismsEvolution is a historical science, and it is important to consider the growth of biological thought and avoid unnecessary redefinitions of established concepts if we are to advance our understanding of complicated issues and circumvent unnecessary controversy. The causes and consequences of discontinuous phenotypic variation and the possible benefits for polymorphic populations and species were much discussed by evolutionary biologists more than half a century ago (e.g. Bateson 1894; Ford 1940Ford , 1945Ford , 1965Dobzhansky 1951;Cain & Sheppard 1954;Huxley 1955;Fisher 1958;Mayr 1963). Interest in the adaptive value of polymorphisms from the point of view of populations thereafter dropped, perhaps in part because the critique and misunderstandings regarding group selection (reviewed in Wilson & Wilson 2007) discouraged students and hampered progress.Research on colour polymorphism as such has grown tremendously both in absolute terms, from <10 papers published per year from 1958 to 1992 to nearly 100 papers in 2014, and relative to total scientific output (Fig. 1). Much of this literature concerns questions related to individual level selection, adaptation and the maintenance of genetic polym...

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“…Still, populations of many species are polymorphic for inherited traits that are likely to affect individual fitness, such as colour. Why species are polymorphic for colour and how this will influence their evolution are not at all clear (Wellenreuther et al , 2014; Bolton et al , 2015). 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).…”

Section: Introductionmentioning

confidence: 99%

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

Johannesson

Butlin

2016

Heredity

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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.

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The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species

Cited by 28 publications

References 132 publications

Back to basics: using colour polymorphisms to study evolutionary processes

Back to basics: using colour polymorphisms to study evolutionary processes

Is colour polymorphism advantageous to populations and species?

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

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