Biology and Environmental Sciences
Being complex can be safe: testing predator avoidance of varying aposematic signals in a novel environment
Author(s): Rojas, B, Rautiala, P, Mappes, J
Conspicuous colour patterns may function as interspecific signals in the context of predation by warning predators about prey unprofitability (aposematism). This strategy relies on the ability of predators to learn the association between colouration and unprofitability, and the subsequent avoidance of the unprofitable prey. Frequency-dependent selection is expected to favour uniformity and act against variability in aposematic signals. However, variation in aposematic species occurs in many taxa suggesting that signal variation may serve other purposes or be under variable selective pressures. Although the fundamental assumptions of aposematism have been well supported by mathematical models and experiments in controlled laboratory setups, their implications in the natural environment of both predators and prey have been until recently greatly overlooked. Predators are supposed to learn simpler patterns easier. Because variation in aposematic signals may imply morph-specific attack rates, aposematism as an anti-predator strategy could be overall less effective for individuals with complex colour patterns, especially when exposed to naïve predators or when invading novel environments, unless there were associated differences in detectability. We tested that hypothesis using wax models of the polymorphic, aposematic poison frog Dendrobates tinctorius placed in the wild, in a site where the actual frogs do not occur. We found that over time aposematic prey get less attacks than cryptic prey, but there were no differences in the attack rate between simple and complex morphs. However, complex morphs seemed to be more difficult to detect than simple ones. We suggest that wild predators are able to generalise aposematic colour patterns. Complex patterns may compensate being difficult to learn by being less detectable, which may contribute to the maintenance of the great intra-populational variation in colour patterns in this species.
Defining the regulatory regions that control Heliconius butterfly colour pattern mimicry
Author(s): Jiggins, CD, Baxter, SW, Wallbank, R, Martin, S, Nadeau, N
Genomic studies of natural populations are offering novel insights into adaptation and diversification. In particular, recent studies of parallel evolution of similar phenotypes in divergent lineages have commonly shown the utilization of shared genetic variation. Heliconius butterflies represent a recently documented example of shared allelic variation across species boundaries.
Heliconius display bright wing patterns that warn predators of distastefulness and also act as mating cues. The diversity of patterns displayed within and between the hundreds of forms is remarkable, as is the convergence between species onto near-perfect mimetic patterns. Recent field studies have identified a group of populations along the eastern slopes of the Andes that are allied to H. timareta and share wing phenotypes with sympatric H. melpomene. Genomic studies have shown that the populations with similar phenotypes also share allelic variation at wing patterning loci, with adaptive introgression across the species boundary providing the most likely explanation for this pattern.
We sequenced a 600 Kb genomic region that regulates diverse red wing pattern phenotypes, using 80 Heliconius samples. Genomic intervals associated with at least three independent red colour pattern phenotypes were resolved using sequence comparisons that grouped similar wing phenotypes, irrespective of species. By comparing the level of nucleotide variation within each colour pattern interval, we estimate the time in generations when introgression events occurred between H. melpomene and H. timareta. Gene exchange after speciation has resulted in the adaptive spread of colour pattern alleles. Here we have identified narrow genomic regions that must act through cis-regulatory control of the transcription factor optix, in order to control complex phenotypes.
Department of Biology
Differential effects of pigmentary and non-pigmentary antioxidants on growth, plumage coloration and resistance to oxidative stress in wild great tits
Author(s): Marri, V, Richner, H
Carotenoid-based colorations are thought to be honest signals of individual quality but the mechanism underlying their expression is still not clear. Since carotenoids act both as antioxidants and immunostimulants, it has been suggested that carotenoid-based coloration can signal an individual’s ability to resist oxidative stress and/or to mount an immune response. However, the antioxidant role of carotenoids in vivo has recently been debated. The "protection hypothesis" holds that carotenoids, which are minor antioxidants and are bleached by reactive oxygen species, can be used as signals to indicate the availability of non-pigmentary antioxidants (e.g. vitamins) that protect them from oxidation. Here, we evaluated this hypothesis by assessing the interactive effects of carotenoids and vitamins on plumage coloration, oxidative stress, growth and fledging success in nestling great tits. We supplemented nestlings with carotenoids (lutein and zeaxanthin) and/or vitamins (E and C) in a 2x2 full-factorial design, and subsequently measured plumage reflectance, antioxidant capacity, oxidative damage and body condition. Vitamins enhanced the expression of the carotenoid-based plumage coloration during the breeding season and improved antioxidant capacity. They did not influence oxidative damage, probably because supplied nestlings invested more in growth, which is a major cause of free-radical production, rather than in reducing oxidative damage. Moreover, vitamin-treated nestlings had a higher probability of fledging. In contrast, carotenoids did not influence any of these traits and did not show any synergistic effect when supplemented together with vitamins. Our results support the "protection hypothesis" and hence the idea that carotenoids are minor antioxidants in vivo. Furthermore, we could show the importance of antioxidants during growth, supporting the idea that oxidative stress may play a central role in life-history trade-offs.
Evolutionary Ecology Unit, Department of Biology
Ecology and mating interactions: temperature influences male-female conflict in a colour polymorphic damselfly
Author(s): Svensson, E
Heritable and conspicuous colour polymorphisms have a long research tradition in ecological genetics, and these systems have been used to investigate issues such as negative-frequency-dependent selection (NFDS), maintenance of genetic variation, sexual selection and sexual conflict. Here I will present long-term field observational data and experiments on the evolutionary dynamics of a sexually selected colour polymorphism in the damselfly Ischnura elegans. Three female morphs exist in this species, one of them being a male mimic ("androchrome females"). Androchrome have lower mating rates than other female morphs, suggesting that male mimicry is a female defence against excessive and costly male mating harassment that is detrimental to female fitness. I will present long-term field data from a longitudinal study across multiple populations that show the stability of this female polymorphism and the results of experiments where we have manipulated morph frequencies and densities and evaluated the effects on morph and population fitnesses. I will also present data showing that the male-female mating interactions are environment-dependent and moulded by ambient temperatures, resulting in geographic variation in morph frequencies. Thus, sexual conflict in this system and the benefits of male mimicry is highly context-dependent upon local ecology and the thermal environment.
Centro de Biologia Ambiental
Experimental and genomic approaches in the study of the balanced colour-polymorphism of the meadow spittlebug (Philaenus spumarius)
Author(s): Seabra, SG, Rodrigues, AS, Silva, SE, Silva, J, Marabuto, E, Pina-Martins, F, Gharbi, K, Blaxter, M, Borges, PAV, Jiggins, C, Quartau, JA, Paulo, OS
Philaenus spumarius (Insecta, Hemiptera, Aphrophoridae) has for long been a subject of interest of evolutionary biologists due to its heritable colour polymorphism that shows evidence of balancing selection and of clinal variation in the colour mophs frequencies. We are studying the adaptive significance of this polymorphism, particularly to understand if the melanic morphs (e.g. “marginellus” morph) have any advantage/disadvantage in terms of survival and reproductive success, efficiency of egg maturation and resistance to desiccation compared to non-melanic morphs (“typicus” and “trilineatus”). Results so far indicate a higher survival, higher number of eggs clutches and higher number of eggs laid by the “trilineatus” females than “typicus” or “marginellus” females. We are also taking a genomic approach for a) the identification of genetic basis of the colour polymorphism and b) for detecting signatures of balancing and directional selection in the genome of P. spumarius. For this purpose we are applying RAD sequencing in a) a set of samples from the three different morphs referred above, using a high frequency cutter enzyme (PstI) and in b) another set of samples from 8 populations across the distribution range of the species representing the main mitochondrial haplogroups, using a lower frequency cutter enzyme (SbfI). We are also assembling a draft of the genome that will aid in the identification of homologous regions to available references, although the very large genome size of this insect constitutes an extra challenge.
Department of Ecology and Evolution
Expression levels of genes belonging to the melanocortin system are associated with melanin-based coloration in two colour polymorphic owl species
Author(s): Roulin, A, Ducrest, A
The adaptive function of colour polymorphism is a long-standing debate, principally because of limited knowledge of the genetic mechanism underlying morph production. A recent genetic model suggested that the melanocortin system could account for covariations between melanin-based colour morphs, behaviour, morphology and physiology. This genetic system may therefore account for the observed morph-specific life history strategies. In two owl species we explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1, PC2 and the antagonist ASIP) as well as 15 other melanogenic genes are associated with melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish. We measured gene expression in feather follicles collected in nestlings at the time of melanin production. Our results are consistent with a key role of the melanocortin system on the expression of colour morphs. We indeed found that the expression levels of convertases (that process melanocortin hormones) covary with melanin-based coloration, an effect that strongly depends on genetic polymorphism at the melanocortin-1-receptor (MC1R). We conclude that the melanocortin system may explain why dark and light melanic morphs adopt alternative life history strategies and differentially cope with stressful factors.
Floral pigmentation evolution and movement through genetic space in snapdragons (Antirrhineae)
Author(s): Ellis, T
Floral pigmentation is a conspicuous and variable trait with an enormous effect on sexual selection, and the underlying genetic pathways are well-understood. As such, flower colour evolution has great potential to inform our understanding of the relationship between genes and phenotype. Previous work has found consistent patterns of irreversible transitions from purple to white, red and blue flowers, via single-locus loss-of-function mutations in regulatory genes of the flavonoid pathway. Since yellow pigmentation is typically controlled by a wholly different pathway, transitions to yellow must involve mutations at two loci. However, transitions involving yellow flowers, or at broader taxonomic scales have never been properly examined. I present results from an ongoing comparative study of floral evolution in a tribe of snapdragons (Antirrhineae, Plantaginaceae), which aims to assess patterns of evolution between yellow, white and purple flowered species in a phylogenetic context. Single locus transitions appear to dominate at short time scales, demonstrating the need to look beyond the genus level. Transitions also appear to be generally more reversible than in previously examined groups. I also examine the role of other floral traits that may be correlated with shifts in flower colour.
Department of Evolutionary Biology
Flower colour morphs of Iris pumila differ in the amounts of Hsp90 and phenolic compounds
Author(s): Tucić, B, Manitašević Jovanović, S, Vuleta, A
Natural populations of the dwarf bearded iris, Iris pumila, display a striking flower-colour polymorphism. It was noted that the combination of fluctuating temperatures and the varied attractiveness of diverse colour morphs promotes a stable coexistence of multiple colour variants in a population. We have quantified the amounts of Hsp90 and the antioxidants, anthocyanins and total phenolics, in I. pumila flowers. These molecules impact abiotic stress tolerance, ultimately influencing the fitness of individual plants. A total of 100 clones that were raised in a common garden and assessed to different colour classes (dark violet, violet, light violet, dark blue, light blue, yellow/white) were examined. The amounts of two Hsp90 forms, inducible (Hsp90a) and constitutively expressed (Hsp90b) proteins were lowest in yellow and white flowers as compared to other colour classes. In blue flowers, the concentration of Hsp90a was observed to decrease gradually when proceeding from light blue to dark blue variants, whereas an inverse trend was observed in violet-coloured flowers. The concentration of anthocyanins was notably low in white/yellow flowers and in the blue and violet colour classes it progressively increased from light to dark floral morphs. The amounts of total phenolics were highest in the white and yellow colour morphs; they were relatively high in all of the blue variants, and gradually increase from light to dark colour morphs in the violet class. These results suggest that each I. pumila colour genotype is responsible for the production of unique amounts of Hsp90 and phenolics that protect cellular homeostasis under fluctuating temperature conditions within populations.
Department of Animal and Plant Sciences
Genetic and genomic insights into a colour polymorphism of the Gouldian finch (Erythrura gouldiae)
Author(s): Kim, K, Pryke, SR, Griffith, SC, Burke, T
The Red locus of the Gouldian finch Erythrura gouldiae is a pigmentation switch that determines black (melanin) and red (carotenoid) morphs. This locus offers a unique opportunity to investigate the genetic basis and evolutionary history of a sympatric polymorphism for colour that has also been found to be associated with multiple physiological and behavioural differences. We used classical linkage mapping combined with RAD (Restriction site Associated DNA) sequencing and association analysis to localize the locus to a small (65-kb) genomic region. The pattern of nucleotide diversity at the Red locus is characterized as a genomic island that shows significant differentiation and divergence between the black and red haplotypes. Evolutionary theory suggests two distinct hypotheses to explain this pattern. First, sequence divergence may have accumulated within the species due to reduced gene flow between morphs, supported by the observed high degree of pre- and post-zygotic incompatibility, or due to a genomic rearrangement. Second, the sequences may have diverged in isolated lineages, prior to population merger or introgression. We examined the two alternative possibilities by using genetic and genomic tools and assess the evidence for balancing selection.
Department of Biology
Genomic instability in the locus responsible for a conspicuous polychromatism in Nicaraguan Midas Cichlid Fish
Author(s): Härer, A, Henning, F, Meyer, A
Body coloration is polymorphic in many species. It is subject to both natural selection (e.g. cryptic coloration) and sexual selection (e.g. male nuptial coloration). Two extraordinary features of Cichlids are their enormous diversity in coloration and their rapid rates of diversification. Sexual selection on coloration has been proposed to be one of the major forces driving their explosive speciation rates, which makes them an ideal system to study the effects of body coloration on speciation processes. Most of the Nicaraguan lakes are inhabited by two color morphs of Midas cichlids: a barred dark morph, which represents the majority of individuals (~90%), and a gold morph (7 - 10%). All individuals have the normal phenotype at early stages of their life but some lose their dark coloration and become gold. Gold and normal fish mate assortatively and genetic divergence of neutral markers occurs between the two morphs. All of which suggests a role of this trait in the process of incipient speciation. In this study, we characterize the architecture of the genomic region that harbors the causal gold polymorphism. The interval was reduced to approximately 60 kb and it, as well as the flanking regions, shows strong evidence of genomic instability. This includes several indels of various sizes, gene duplications and chromosomal rearrangements. Lineage-specific, tandemly duplicated genes have been identified, some of which show signs of pseudogenization and selection. Comparative genomic analysis of the region indicates the presence of cichlid-specific and perhaps even Midas-specific chromosomal rearrangements. Regions of genomic instability have been proposed to have an impact on speciation due to altered recombination and mutation rates. The present study illustrates the architecture of an unstable genomic region that might underlie incipient sympatric speciation in Nicaraguan Midas cichlids.