Towards a theory of the evolution of butterfly colour patterns under directional and disruptive selection

Two general models for the transspecific evolution of butterfly colour patterns are advanced: directional selection acting equally on both sexes, and disruptive selection involving periods of polymorphism. To consider possible outcomes of me latter process, a morphism notation based on an integrated classification for polymorphism and sexual dimorphism is developed. This notation is used to examine the properties of all morphism transformations possible from the minimal expressions of the nine morphism categories, as reached through defined minimum step changes. The significance of such pathway models is analysed in terms of general properties of butterfly polymorphism. The potential use of pathway models in evolutionary studies is briefly discussed, mainly with respect to phylogenetics, and ideas on the evolution of genetic dominance.     

Crypsis in a heterogeneous environment: relationships between changeable polymorphic colour patterns and behaviour in a galaxiid fish

1. The ability to achieve optimal camouflage varies between microhabitats in heterogeneous environments, potentially restricting individuals to a single habitat or imposing a compromise on crypsis to match several habitats. However, animals may exhibit morphological and behavioural attributes that enhance crypsis in different habitats. 2. We used an undescribed fish species, Galaxias‘nebula’, to investigate two objectives. First, we examined two potential methods of enhancing crypsis: change in colour pattern and selection of a suitable background. Second, we characterised the colour pattern of this unstudied fish and assessed its capacity for crypsis. 3. No background selection was apparent but the area of dark pigment expressed varied between backgrounds, which may negate the requirement to be choosy about habitats. The capacity to change colour and selection of a background that maximises crypsis are most likely separate, non‐mutually exclusive strategies. 4. Galaxias‘nebula’ exhibits polymorphic, non‐interchangeable colour patterns that have elements of both background pattern matching and disruptive colouration. This, coupled with habitat characteristics, suggests a combination of generalist and specialist strategies of habitat use. The fish’s camouflage strategy and air‐breathing ability may be key to survival under increasing pressure from habitat degradation and invasive predators.     

Extra-pair paternity and sexual dimorphism in birds

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.     

Geographic variation for colour in the sandburrowing beetle Chaerodes trachyscelides White (Goleoptera: Tenebrionidae) on New Zealand beaches analysed using CIELAB L * values

Chaerodes trachyscelides White is a highly specialized, flightless burrowing beetle confined to the narrow strip of sand at and just above high water level on sandy marine beaches in New Zealand. Although the ventral surface of the beetle is always pale, the dorsal surface varies from pale to almost black. Large samples of this beetle were taken, together with the sand, from 11 beaches on New Zealand's three main islands. The colour of the dorsal surface of each individual beetle and that of the sand samples was measured using reflectance spectroscopy and expressed as CIE L*,a*,b* (CIELAB) values. The L* values, which are objective, quantitative measures of the degree of lightness of the beetles, were subjected to statistical and frequency analysis. Although the species was very variable in colour and the variation appeared to be continuous, a highly significant correlation was obtained between the mean of the L* values for the samples on each beach and that of the sand, the correlation coefficient being 0.961. This close association between the lightness of the beetles and that of the sand suggests the variable melanism functions as cryptic colouration. On most beaches, the distribution oflightness among the beetles sampled conformed to a normal curve. For beetles from sites where the sand was relatively uniform, such as the black Taranaki beaches, the L* frequency distribution curves were narrow and the coefficient of variation of mean beetle colour was relatively small indicating low colour variability. In contrast, the greatest within-site variability occurred on the two Stewart Island beaches sampled, where in each case there was less uniformity in the colour of the sand. At one of these sites, Maori Beach, darker sand present below the high water level is often deposited on the zone occupied by the beetles after storms. On Lonneker's Beach, the distribution of L* values among the beetles sampled was actually bimodal. On this small beach, there was an area of intensely black sand in the zone occupied by the beetles, but most of the rest was covered with light golden sand. These results are interpreted as evidence that the variability of colour of Chaerodes beetles has the effect of populations being able to match the colour of the sand of their home beaches, presumably as a consequence of the differential survival of individuals.     

Innate colour preferences of flower visitors

Freshly emerged flower visitors exhibit colour preferences prior to individual experience with flowers. The understanding of innate colour preferences in flower visitors requires a detailed analysis, as, on the one hand, colour is a multiple-signal stimulus, and, on the other hand, flower visits include a sequence of behavioural reactions each of which can be driven by a preferential behaviour. Behavioural reactions, such as the distant approach, the close-range orientation, the landing, and the extension of mouthparts can be triggered by colour stimuli. The physiological limitations of spectral sensitivity, the neuro-sensory filters, and the animals' different abilities to make use of visual information such as brightness perception, wavelength-specific behaviour and colour vision shape colour preferences. Besides these receiverbased factors, there are restrictions of flower colouration due to sender-based factors such as the absorption properties of floral pigments and the dual function of flower colours triggering both innate and learned behaviour. Recordings of the spectral reflection of coloured objects, which trigger innate colour preferences, provide an objective measure of the colour stimuli. Weighting the spectral reflection of coloured objects by the spectral composition of the ambient light and the spectral sensitivity of the flower visitors' photoreceptors allows the calculation of the effective stimuli. Perceptual dimensions are known for only a few taxa of flower visitors.     

Evolution of dispersal in spatially and temporally variable environments: The importance of life cycles

Spatiotemporal variability of the environment is bound to affect the evolution of dispersal, and yet model predictions strongly differ on this particular effect. Recent studies on the evolution of local adaptation have shown that the life cycle chosen to model the selective effects of spatiotemporal variability of the environment is a critical factor determining evolutionary outcomes. Here, we investigate the effect of the order of events in the life cycle on the evolution of unconditional dispersal in a spatially heterogeneous, temporally varying landscape. Our results show that the occurrence of intermediate singular strategies and disruptive selection are conditioned by the temporal autocorrelation of the environment and by the life cycle. Life cycles with dispersal of adults versus dispersal of juveniles, local versus global density regulation, give radically different evolutionary outcomes that include selection for total philopatry, evolutionary bistability, selection for intermediate stable states, and evolutionary branching points. Our results highlight the importance of accounting for life‐cycle specifics when predicting the effects of the environment on evolutionarily selected trait values, such as dispersal, as well as the need to check the robustness of model conclusions against modifications of the life cycle.     

Stabilizing survival selection on presenescent expression of a sexual ornament followed by a terminal decline

Senescence is a decrease in functional capacity, increasing mortality rate with age. Sexual signals indicate functional capacity, because costs of ornamentation ensure signal honesty, and are therefore expected to senesce, tracking physiological deterioration and mortality. For sexual traits, mixed associations with age and positive associations with life expectancy have been reported. However, whether these associations are caused by selective disappearance and/or within‐individual senescence of sexual signals, respectively, is not known. We previously reported that zebra finches with redder bills had greater life expectancy, based on a single bill colour measurement per individual. We here extend this analysis using longitudinal data and show that this finding is attributable to terminal declines in bill redness in the year before death, with no detectable change in presenescent redness. Additionally, there was a quadratic relationship between presenescent bill colouration and survival: individuals with intermediate bill redness have maximum survival prospects. This may reflect that redder individuals overinvest in colouration and/or associated physiological changes, while below‐average bill redness probably reflects poorer phenotypic quality. Together, this pattern suggests that bill colouration is defended against physiological deterioration, because of mate attraction benefits, or that physiological deterioration is not a gradual process, but accelerates sharply prior to death. We discuss these possibilities in the context of the reliability theory of ageing and sexual selection.     

Field and experimental evidence for competition's role in phenotypic divergence

Resource competition has long been viewed as a major cause of phenotypic divergence within and between species. Theory predicts that divergence arises because natural selection favors individuals that are phenotypically dissimilar from their competitors. Yet, there are few conclusive tests of this key prediction. Drawing on data from both natural populations and a controlled experiment, this paper presents such a test in tadpoles of two species of spadefoot toads (Spea bombifrons and S. multiplicata). These two species show exaggerated divergence in trophic morphology where they are found together (mixed-species ponds) but not where each is found alone (pure-species ponds), suggesting that they have undergone ecological character displacement. Moreover, in pure-species ponds, both species exhibit resource polymorphism. Using body size as a proxy for fitness, we found that in pure-species ponds disruptive selection favors extreme trophic phenotypes in both species, suggesting that intraspecific competition for food promotes resource polymorphism. In mixed-species ponds, by contrast, we found that trophic morphology was subject to stabilizing selection in S. multiplicata and directional selection in S. bombifrons. A controlled experiment revealed that the more similar an S. multiplicata was to its S. bombifrons tankmate in resource use, the worse was its performance. These results indicate that S. multiplicata individuals that differ from S. bombifrons would be selectively favored in competition. Our data therefore demonstrate how resource competition between phenotypically similar individuals can drive divergence between them. Moreover, our results indicate that how competition contributes to such divergence may be influenced not only by the degree to which competitors overlap in resource use, but also by the abundance and quality of resources. Finally, our finding that competitively mediated disruptive selection may promote resource polymorphism has potentially important implications for understanding how populations evolve in response to heterospecific competitors. In particular, once a population evolves resource polymorphism, it may be more prone to undergo ecological character displacement.     

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.