Is colour polymorphism advantageous to populations and species?

Abstract

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...

Faster poleward range shifts in moths with more variable colour patterns

“…There is experimental and comparative evidence from a broad range of taxonomic groups that species with more variable colour patterns have larger range sizes, higher establishment success, and lower extinction risk2024252627. However, we are not aware of any previous demonstration that species with more variable colour patterns have undergone faster range shifts.…”

“…Northerly range limits decreased with increasing year-to-year changes in abundance (1973: r  = −0.25, n  = 236, P  = 0.0001; 2014: r  = −0.26, n  = 240, P  < 0.0001), suggesting that a high ability to cope with environmental change allows for more northerly distributions, and that poorly buffered species cannot readily establish in areas with harsh climate conditions. Northern boundaries also increased with increasing average abundance (1973: r  = 0.22, n  = 236, P  = 0.0008; 2014: r  = 0.22, n  = 240, P  = 0.0005), perhaps reflecting that species with high population densities produce more long-distance dispersers, or are less likely to go extinct once established2027.…”

“…Furthermore, colour patterns are genetically and developmentally associated with other phenotypic dimensions, such as body size, disease resistance, reproductive life-history traits, microhabitat use and diet1819. Because of the associations of coloration with several other traits, it has been hypothesized that higher levels of inter-individual variation in colour pattern can be considered a proxy of ecological generalization that enables populations and species to utilize broader niches18, and that colour polymorphism may therefore allow for more efficient utilization of diverse resources, reduce vulnerability to environmental change, contribute to higher and more stable population densities, which in turn should promote establishment success, and reduce extinction rate1820. Variable coloration can also protect prey populations against predation21.…”

“…Variable coloration can also protect prey populations against predation21. As a consequence, species with variable colour patterns should be capable of faster range expansions compared with species that do not vary in colour pattern, due to mechanisms operating on colour pattern as such, as well as to processes involving traits that are associated with colour pattern1820.…”

On the role of sex differences for evolution in heterogeneous and changing fitness landscapes: insights from pygmy grasshoppers

“…In addition, it can have important population-level consequences [3,55,88–90], for example, by lessening the negative effects of intra-specific competition [91], reducing predation [92,93] and improving establishment success in novel areas [94]. But the polymorphic condition in PGHs goes beyond colour patterns, it applies also to dispersal.…”