Tests of search image and learning in the wild: Insights from sexual conflict in damselflies

Search image formation, a proximal mechanism to maintain genetic polymorphisms by negative frequency‐dependent selection, has rarely been tested under natural conditions. Females of many nonterritorial damselflies resemble either conspecific males or background vegetation. Mate‐searching males are assumed to form search images of the majority female type, sexually harassing it at rates higher than expected from its frequency, thus selectively favoring the less common morph. We tested this and how morph coloration and behavior influenced male perception and intersexual encounters by following marked Ischnura elegans and noting their reactions to conspecifics. Contrary to search image formation and associative learning hypotheses, although males encountered the minority, male‐like morph more often, sexual harassment and clutch size were similar for both morphs. Prior mating attempts or copula with morphs did not affect a male''s subsequent reaction to them; males rarely attempted matings with immature females or males. Females mated early in the day, reducing the opportunity for males to learn their identity beforehand. Once encountered, the male‐like morph was more readily noticed by males than the alternative morph, which once noticed was more likely to receive mating attempts. Flexible behavior gave morphs considerable control over their apparency to males, influencing intersexual encounters. Results suggested a more subtle proximal mechanism than male learning maintains these color polymorphisms and call for inferences of learning to be validated by behavior of wild receivers and their signalers.     

Museomics Dissects the Genetic Basis for Adaptive Seasonal Coloration in the Least Weasel

Dissecting the link between genetic variation and adaptive phenotypes provides outstanding opportunities to understand fundamental evolutionary processes. Here, we use a museomics approach to investigate the genetic basis and evolution of winter coat coloration morphs in least weasels (Mustela nivalis), a repeated adaptation for camouflage in mammals with seasonal pelage color moults across regions with varying winter snow. Whole-genome sequence data were obtained from biological collections and mapped onto a newly assembled reference genome for the species. Sampling represented two replicate transition zones between nivalis and vulgaris coloration morphs in Europe, which typically develop white or brown winter coats, respectively. Population analyses showed that the morph distribution across transition zones is not a by-product of historical structure. Association scans linked a 200-kb genomic region to coloration morph, which was validated by genotyping museum specimens from intermorph experimental crosses. Genotyping the wild populations narrowed down the association to pigmentation gene MC1R and pinpointed a candidate amino acid change cosegregating with coloration morph. This polymorphism replaces an ancestral leucine residue by lysine at the start of the first extracellular loop of the protein in the vulgaris morph. A selective sweep signature overlapped the association region in vulgaris, suggesting that past adaptation favored winter-brown morphs and can anchor future adaptive responses to decreasing winter snow. Using biological collections as valuable resources to study natural adaptations, our study showed a new evolutionary route generating winter color variation in mammals and that seasonal camouflage can be modulated by changes at single key genes.     

Camouflage versus running performance as strategies against predation in a lizard inhabiting different habitats

Running speed and camouflage are associated with the foraging and anti‐predator abilities of animals. The toad‐headed lizard, Phrynocephalus versicolor, has evolved a darker dorsal color in melanistic habitats and maintained a lighter color in adjacent, non‐melanistic habitats. We test the hypothesis that lizards have weaker running speed on well‐matching backgrounds than on less matching backgrounds. We used lizard models to compare the predation pressure, while the running speed of dark and light lizards were compared in field tunnels using a video recording method. Our results indicated that both the dark lizards in melanistic Heishankou (HSK) and the light lizards in non‐melanistic Guazhou (GZ) face lower predation pressure than potential color‐background unmatched lizards. The light lizards have a potentially higher running speed than darker lizards in melanistic habitats, which implies that substrate color matching populations with benefits of camouflage might have lower anti‐predation pressure, and the costs of investment in melanin production may reduce running capacity.     

Low genome‐wide divergence between two lizard populations with high adaptive phenotypic differentiation

Usually, adaptive phenotypic differentiation is paralleled by genetic divergence between locally adapted populations. However, adaptation can also happen in a scenario of nonsignificant genetic divergence due to intense gene flow and/or recent differentiation. While this phenomenon is rarely published, findings on incipient ecologically driven divergence or isolation by adaptation are relatively common, which could confound our understanding about the frequency at which they actually occur in nature. Here, we explore genome‐wide traces of divergence between two populations of the lacertid lizard Psammodromus algirus separated by a 600 m elevational gradient. These populations seem to be differentially adapted to their environments despite showing low levels of genetic differentiation (according to previously studies of mtDNA and microsatellite data). We performed a search for outliers (i.e., loci subject to selection) trying to identify specific loci with F_ST statistics significantly higher than those expected on the basis of overall, genome‐wide estimates of genetic divergence. We find that local phenotypic adaptation (in terms of a wide diversity of characters) was not accompanied by genome‐wide differentiation, even when we maximized the chances of unveiling such differentiation at particular loci with F_ST‐based outlier detection tests. Instead, our analyses confirmed the lack of genome‐wide differentiation on the basis of more than 70,000 SNPs, which is concordant with a scenario of local adaptation without isolation by environment. Our results add evidence to previous studies in which local adaptation does not lead to any kind of isolation (or early stages of ecological speciation), but maintains phenotypic divergence despite the lack of a differentiated genomic background.     

THE STRIPED COLOUR PATTERN AND STRIPED/NON-STRIPED POLYMORPHISM IN SNAKES (REPTILIA: OPHIDIA)*

The occurrence of striped colour patterns and of striped/non-striped polymorphism systems among snakes is reviewed from literature data augmented by some personal observations. Among 1367 species, 190 were striped or had striped morphs. Of 11 families, the striped pattern was common mainly among Colubridae, presumably in relation to the active escape behaviour strategy, prevalent in this family. The striped species tended to cluster in a small number of genera. The 40 striped/non-striped polymorphism systems found, fall into five categories, according to the coloration patterns of the alternative morphs: (I) blotched (cryptic); (2) barred (or ringed); (3) plain; (4) melanistic; (5) albinistic. Most polymorphisms are presumably maintained by eco-behavioural trade-offs, depending on the category and on the habitat: The striped morph is presumed more effective in active escape and sometimes also in camouflage; the alternative morph may be more effective in camouflage, in active escape or in thermoregulation. Hence morph frequency depends on the habitat. Striped-albinistic polymorphism in Elaphe climacophora presumably depends on human protection of the albino morph.     

Phenotypic plasticity in insects: the effects of substrate color on the coloration of two ground-hopper species

SUMMARY The question of how phenotypic variation is maintained within populations has long been a central issue in evolutionary biology. Most of these studies focused on the maintenance of genetic variability, but the phenotype of organisms may also be influenced by environmental cues experienced during ontogeny. Color polymorphism has received particular attention in evolutionary studies as it has strong fitness consequences. However, if body coloration is influenced by the environment, any conclusions on evolutionary consequences of fitness trade-offs can be misleading. Here we present data from a laboratory experiment on the influence of substrate color on three aspects of the coloration of two ground-hopper species, Tetrix subulata and Tetrix ceperoi . We reared hatchlings either on dark or on light substrates, using a split-brood design. Although the type of pronotal pattern changed mainly in response to nymphal development, the basic color was strongly influenced by the substrate color. In both species, black and dark olive color morphs were found more frequently on the dark substrate, whereas the gray color morph dominated on the light substrate. These findings have considerable implications for our understanding of color morph evolution as they show that color polymorphism may not only be maintained by natural selection acting on discrete color morphs, but also by phenotypic plasticity, which enables organisms to adjust to the environmental conditions experienced during ontogeny. This facultative morphology is opposing to the prevailing view of color morph adaptation, which assumes a purely genetic determination and co-evolution of discrete color morphs with life history traits.     

Opposing fitness consequences of colour pattern in male and female snakes

Local populations of the adder, Vipera berus, are polymorphic for dorsal colour pattern, containing both melanistic (black) and zig-zag patterned individuals. Colour patterns in snakes influence crypsis and thermoregulatory capacity and therefore may be subjected to natural selection. To find an explanation for the maintenance of this polymorphism I examined temporal and spatial variation in morph frequency, and tested for differential selection among morphs using data from a six year capture-mark-recapture study. The data derive from six groups of islands in the Baltic Sea off the Swedish east coast, two mainland localities near the coast, and one inland locality. Morph frequency did not change over time within a population but varied among populations: melanistic individuals were not found at the inland locality, but comprised from 17 to 62% of the coastal and island populations. Adders frequently moved between islands within a group, but the tendency to disperse was independent of morph. These results suggest that the polymorphism is stable and maintained by a deterministic process. Scar frequency was twice as high among melanistic as among zig-zag snakes, and melanistic individuals were easier to capture, indicating that predation may be higher on the melanistic morph. Colour morphs did not differ in body size, but analysis of recapture data shows evidence for differential survival among morphs. Zig-zag males survived better than melanistic males, but the relative survival rates of morphs were reversed in females. This difference was consistent through time and may be due to sexual differences in behaviour, with melanism increasing predation intensity when associated with male but not with female behaviour. Opposing fitness consequences of colour pattern in the two sexes may help maintain colour polymorphism within populations of Vipera berus.     

Pigment cell mechanisms underlying dorsal color‐pattern polymorphism in the japanese four‐lined snake

To provide histological foundation for studying the genetic mechanisms of color‐pattern polymorphisms, we examined light reflectance profiles and cellular architectures of pigment cells that produced striped, nonstriped, and melanistic color patterns in the snake Elaphe quadrivirgata. Both, striped and nonstriped morphs, possessed the same set of epidermal melanophores and three types of dermal pigment cells (yellow xanthophores, iridescent iridophores, and black melanophores), but spatial variations in the densities of epidermal and dermal melanophores produced individual variations in stripe vividness. The densities of epidermal and dermal melanophores were two or three times higher in the dark‐brown‐stripe region than in the yellow background in the striped morph. However, the densities of epidermal and dermal melanophores between the striped and background regions were similar in the nonstriped morph. The melanistic morph had only epidermal and dermal melanophores and neither xanthophores nor iridophores were detected. Ghost stripes in the shed skin of some melanistic morphs suggested that stripe pattern formation and melanism were controlled independently. We proposed complete‐ and incomplete‐dominance heredity models for the stripe‐melanistic variation and striped, pale‐striped, and nonstriped polymorphisms, respectively, according to the differences in pigment‐cell composition and its spatial architecture. J. Morphol. 274:1353–1364, 2013. © 2013 Wiley Periodicals, Inc.     

Spectral Sensitivities and Color Signals in a Polymorphic Damselfly

Animal communication relies on conspicuous signals and compatible signal perception abilities. Good signal perception abilities are particularly important for polymorphic animals where mate choice can be a challenge. Behavioral studies suggest that polymorphic damselflies use their varying body colorations and/or color patterns as communication signal for mate choice and to control mating frequencies. However, solid evidence for this hypothesis combining physiological with spectral and behavioral data is scarce. We investigated this question in the Australian common blue tail damselfly, Ischnura heterosticta, which has pronounced female-limited polymorphism: andromorphs have a male-like blue coloration and gynomorphs display green/grey colors. We measured body color reflectance and investigated the visual capacities of each morph, showing that I. heterosticta have at least three types of photoreceptors sensitive to UV, blue, and green wavelength, and that this visual perception ability enables them to detect the spectral properties of the color signals emitted from the various color morphs in both males and females. We further demonstrate that different color morphs can be discriminated against each other and the vegetation based on color contrast. Finally, these findings were supported by field observations of natural mating pairs showing that mating partners are indeed chosen based on their body coloration. Our study provides the first comprehensive evidence for the function of body coloration on mate choice in polymorphic damselflies.     

Species boundaries in the messy middle—A genome‐scale validation of species delimitation in a recently diverged lineage of coastal fog desert lichen fungi

Species delimitation among closely related species is challenging because traditional phenotype‐based approaches, for example, using morphology, ecological, or chemical characteristics, may not coincide with natural groupings. With the advent of high‐throughput sequencing, it has become increasingly cost‐effective to acquire genome‐scale data which can resolve previously ambiguous species boundaries. As the availability of genome‐scale data has increased, numerous species delimitation analyses, such as BPP and SNAPP+Bayes factor delimitation (BFD*), have been developed to delimit species boundaries. However, even empirical molecular species delimitation approaches can be biased by confounding evolutionary factors, for example, hybridization/introgression and incomplete lineage sorting, and computational limitations. Here, we investigate species boundaries and the potential for micro‐endemism in a lineage of lichen‐forming fungi, Niebla Rundel & Bowler, in the family Ramalinaceae by analyzing single‐locus and genome‐scale data consisting of (a) single‐locus species delimitation analysis using ASAP, (b) maximum likelihood‐based phylogenetic tree inference, (c) genome‐scale species delimitation models, e.g., BPP and SNAPP+BFD, and (d) species validation using the genealogical divergence index (gdi). We specifically use these methods to cross‐validate results between genome‐scale and single‐locus datasets, differently sampled subsets of genomic data and to control for population‐level genetic divergence. Our species delimitation models tend to support more speciose groupings that were inconsistent with traditional taxonomy, supporting a hypothesis of micro‐endemism, which may include morphologically cryptic species. However, the models did not converge on robust, consistent species delimitations. While the results of our analysis are somewhat ambiguous in terms of species boundaries, they provide a valuable perspective on how to use these empirical species delimitation methods in a nonmodel system. This study thus highlights the challenges inherent in delimiting species, particularly in groups such as Niebla, with complex, relatively recent phylogeographic histories.     

Flickers of speciation: Sympatric colour morphs of the arc‐eye hawkfish,Paracirrhites arcatus,reveal key elements of divergence with gene flow

One of the primary challenges of evolutionary research is to identify ecological factors that favour reproductive isolation. Therefore, studying partially isolated taxa has the potential to provide novel insight into the mechanisms of evolutionary divergence. Our study utilizes an adaptive colour polymorphism in the arc‐eye hawkfish (Paracirrhites arcatus) to explore the evolution of reproductive barriers in the absence of geographic isolation. Dark and light morphs are ecologically partitioned into basaltic and coral microhabitats a few metres apart. To test whether ecological barriers have reduced gene flow among dark and light phenotypes, we evaluated genetic variation at 30 microsatellite loci and a nuclear exon (Mc1r) associated with melanistic coloration. We report low, but significant microsatellite differentiation among colour morphs and stronger divergence in the coding region of Mc1r indicating signatures of selection. Critically, we observed greater genetic divergence between colour morphs on the same reefs than that between the same morphs in different geographic locations. We hypothesize that adaptation to the contrasting microhabitats is overriding gene flow and is responsible for the partial reproductive isolation observed between sympatric colour morphs. Combined with complementary studies of hawkfish ecology and behaviour, these genetic results indicate an ecological barrier to gene flow initiated by habitat selection and enhanced by assortative mating. Hence, the arc‐eye hawkfish fulfil theoretical expectations for the earliest phase of speciation with gene flow.     

Genetic Structure in a Heterocyanic Population of Trillium sessile (Liliaceae)

Abstract Species of Trillium in the subgenus Phyllantherum are either polymorphic for flower color, or monomorphic for flower color and related to a polymorphic species. This leads to the suggestion that polymorphic species may be the progenitors for monomorphic ones. For this to be true, it must be demonstrated that genetic divergence among flower morphs can occur within polymorphic populations. Genetic structure was assessed in a population of T. sessile that contains a polymorphism for flower color. A survey of 11 enzyme systems using starch gel electrophoresis revealed three polymorphic loci: 6PGD-1, AAT-1 and AAT-2. Analysis of large and small scale spatial structure, stage classes, and flower color classes revealed significant genetic divergence in all instances. Spatial structure in the population is likely a result of genetic neighborhoods which can maintain populational variation via random genetic drift. Genetic divergence of the yellow flower color morph was probably initiated through genetic drift since the morph occurs in low frequencies. The results imply that the initial genetic divergence of species in the subgenus can arise within polymorphic populations.     

A novel resource polymorphism in fish, driven by differential bottom environments: an example from an ancient lake in Japan

Divergent natural selection rooted in differential resource use can generate and maintain intraspecific eco-morphological divergence (i.e., resource polymorphism), ultimately leading to population splitting and speciation. Differing bottom environments create lake habitats with different benthos communities, which may cause selection in benthivorous fishes. Here, we document the nature of eco-morphological and genetic divergence among local populations of the Japanese gudgeon Sarcocheilichthys (Cyprinidae), which inhabits contrasting habitats in the littoral zones (rocky vs. pebbly habitats) in Lake Biwa, a representative ancient lake in East Asia. Eco-morphological analyses revealed that Sarcocheilichthys variegatus microoculus from rocky and pebbly zones differed in morphology and diet, and that populations from rocky environments had longer heads and deeper bodies, which are expected to be advantageous for capturing cryptic and/or attached prey in structurally complex, rocky habitats. Sarcocheilichthys biwaensis, a rock-dwelling specialist, exhibited similar morphologies to the sympatric congener, S. v. microoculus, except for body/fin coloration. Genetic analyses based on mitochondrial and nuclear microsatellite DNA data revealed no clear genetic differentiation among local populations within/between the gudgeon species. Although the morphogenetic factors that contribute to morphological divergence remain unclear, our results suggest that the gudgeon populations in Lake Biwa show a state of resource polymorphism associated with differences in the bottom environment. This is a novel example of resource polymorphism in fish within an Asian ancient lake, emphasizing the importance and generality of feeding adaptation as an evolutionary mechanism that generates morphological diversification.     

Fruit color,chemical and genetic diversity and structure of Myrtus communis L. var. italica Mill. morph populations

Myrtus communis presents two morphologies based on fruit color. Both morphs are present in some region of Tunisia, with the white morph being rare. In the present study, essential oil composition and AFLP markers were used to assess the chemical and genetic diversity and structure of four myrtle populations from each morph. A chemical polymorphism attributed to the morphs and the origin of populations was detected.The genetic diversity within population varied according to morphs. Variation in the dark blue morph populations was higher than that observed for the white ones. For each morph, a high genetic differentiation among populations was observed. Population structure based on AFLP markers is in accordance with that based on oil composition. Furthermore, a significant correlation between chemical and genetic data was observed. The conservation strategies of populations should be made for each morph according to its level of diversity and bioclimate.     

Variation in parasite resistance of Arctic charr,Salvelinus alpinus,between and within sympatric morphs

Genetic variation in resistance against parasite infections is a predominant feature in host–parasite systems. However, mechanisms maintaining genetic polymorphism in resistance in natural host populations are generally poorly known. We explored whether differences in natural infection pressure between resource‐based morphs of Arctic charr (Salvelinus alpinus) have resulted in differentiation in resistance profiles. We experimentally exposed offspring of two morphs from Lake Þingvallavatn (Iceland), the pelagic planktivorous charr (“murta”) and the large benthivorous charr (“kuðungableikja”), to their common parasite, eye fluke Diplostomum baeri, infecting the eye humor. We found that there were no differences in resistance between the morphs, but clear differences among families within each morph. Moreover, we found suggestive evidence of resistance of offspring within families being positively correlated with the parasite load of the father, but not with that of the mother. Our results suggest that the inherited basis of parasite resistance in this system is likely to be related to variation among host individuals within each morph rather than ecological factors driving divergent resistance profiles at morph level. Overall, this may have implications for evolution of resistance through processes such as sexual selection.     

Pollinator Competition as a Driver of Floral Divergence: An Experimental Test

Optimal foraging models of floral divergence predict that competition between two different types of pollinators will result in partitioning, increased assortative mating, and divergence of two floral phenotypes. We tested these predictions in a tropical plant-pollinator system using sexes of purple-throated carib hummingbirds (Anthracothorax jugularis) as the pollinators, red and yellow inflorescence morphs of Heliconia caribaea as the plants, and fluorescent dyes as pollen analogs in an enclosed outdoor garden. When foraging alone, males exhibited a significant preference for the yellow morph of H. caribaea, whereas females exhibited no preference. In competition, males maintained their preference for the yellow morph and through aggression caused females to over-visit the red morph, resulting in resource partitioning. Competition significantly increased within-morph dye transfer (assortative mating) relative to non-competitive environments. Competition and partitioning of color morphs by sexes of purple-throated caribs also resulted in selection for floral divergence as measured by dye deposition on stigmas. Red and yellow morphs did not differ significantly in dye deposition in the competition trials, but differences in dye deposition and preferences for morphs when sexes of purple-throated caribs foraged alone implied fixation of one or the other color morph in the absence of competition. Competition also resulted in selection for divergence in corolla length, with the red morph experiencing directional selection for longer corollas and the yellow morph experiencing stabilizing selection on corolla length. Our results thus support predictions of foraging models of floral divergence and indicate that pollinator competition is a viable mechanism for divergence in floral traits of plants.     

RAD sequencing of common whelk,Buccinum undatum,reveals fine‐scale population structuring in Europe and cryptic speciation within the North Atlantic

Buccinum undatum is a subtidal gastropod that exhibits clear spatial variation in several phenotypic shell traits (color, shape, and thickness) across its North Atlantic distribution. Studies of spatial phenotypic variation exist for the species; however, population genetic studies have thus far relied on a limited set of mitochondrial and microsatellite markers. Here, we greatly expand on previous work by characterizing population genetic structure in B. undatum across the North Atlantic from SNP variation obtained by RAD sequencing. There was a high degree of genetic differentiation between Canadian and European populations (Iceland, Faroe Islands, and England) consistent with the divergence of populations in allopatry (F _ST > 0.57 for all pairwise comparisons). In addition, B. undatum populations within Iceland, the Faroe Islands, and England are typified by weak but significant genetic structuring following an isolation‐by‐distance model. Finally, we established a significant correlation between genetic structuring in Iceland and two phenotypic traits: shell shape and color frequency. The works detailed here enhance our understanding of genetic structuring in B. undatum and establish the species as an intriguing model for future genome‐wide association studies.     

Trophic polymorphism, habitat and diet segregation in Percichthys trucha (Pisces: Percichthyidae) in the Andes

Divergent natural selection affecting specific trait combinations that lead to greater efficiency in resource exploitation is believed to be a major mechanism leading to trophic polymorphism and adaptive radiation. We present evidence of trophic polymorphism involving two benthic morphs within Percichthys trucha , a fish endemic to temperate South America. In a series of lakes located in the southern Andes, we found two morphs of P. trucha that could be distinguished on the basis of gill raker length and five other morphological measures, most of which are likely associated with the use of food resources. The differences were consistent across all lakes examined, and were correlated with habitat use and diet. Individuals with longer gill rakers were more abundant in the littoral zone (littoral morph) while the short gill-raker morph was more abundant at 10 m depth and deeper (deep benthic morph). Both morphs fed primarily on benthic invertebrates, but the littoral morph fed more on larval Anisoptera than did the deep benthic morph. Phenotypic correlations among traits were high for the littoral morph, but low and non-significant for the deep-benthic morph. We suggest that gill raker length may influence the relative efficiency of suction feeding for the two morphs. This is the first evidence of trophic polymorphism in fishes from temperate South America.     

Adaptive Radiation along a Thermal Gradient: Preliminary Results of Habitat Use and Respiration Rate Divergence among Whitefish Morphs

Adaptive radiation is considered an important mechanism for the development of new species, but very little is known about the role of thermal adaptation during this process. Such adaptation should be especially important in poikilothermic animals that are often subjected to pronounced seasonal temperature variation that directly affects metabolic function. We conducted a preliminary study of individual lifetime thermal habitat use and respiration rates of four whitefish (Coregonus lavaretus (L.)) morphs (two pelagic, one littoral and one profundal) using stable carbon and oxygen isotope values of otolith carbonate. These morphs, two of which utilized pelagic habitats, one littoral and one profundal recently diverged via adaptive radiation to exploit different major niches in a deep and thermally stratified subarctic lake. We found evidence that the morphs used different thermal niches. The profundal morph had the most distinct thermal niche and consistently occupied the coldest thermal habitat of the lake, whereas differences were less pronounced among the shallow water pelagic and littoral morphs. Our results indicated ontogenetic shifts in thermal niches: juveniles of all whitefish morphs inhabited warmer ambient temperatures than adults. According to sampling of the otolith nucleus, hatching temperatures were higher for benthic compared to pelagic morphs. Estimated respiration rate was the lowest for benthivorous profundal morph, contrasting with the higher values estimated for the other morphs that inhabited shallower and warmer water. These preliminary results suggest that physiological adaptation to different thermal habitats shown by the sympatric morphs may play a significant role in maintaining or strengthening niche segregation and divergence in life-history traits, potentially contributing to reproductive isolation and incipient speciation.