Does soil color affect fish evolution? Differences in color change rate between lineages of the sailfin tetra

ABSTRACT Several organisms match their skin color to the prevalent background color, granting crypsis against predators. The rate at which body color changes occur varies among organisms as a result of physiological constraints and adaptation to variation in contrasts between objects and the environmental background. Faster darkening of body color is favored in environments that show higher amounts of contrast between common objects and the prevailing background. Soil types in Amazon forest streams (igarapés) create distinct environments with respect to the amount of contrast, a result of the amount of sand and clay, which offers different contrasts against dead leaves. Here, we investigated differences in the rates of color change among populations of the sailfin tetra (Crenuchus spilurus) that represent lineages that live in regions of different soil types. Populations inserted into blackwaters (sandy soil) showed higher rates of color darkening in response to exposure to a dark environment composed by dead leaves. We propose that natural selection stemming from predation can favor faster color change rate in environments where there is higher variability of contrasts between leaf litter and soil, which is common in most blackwater streams.

RESUMO Diversos organismos combinam sua coloração corporal com a cor de fundo predominante no ambiente, conferindo cripticidade contra predadores. A taxa na qual as mudanças de coloração corpórea ocorrem varia entre os organismos como resultado de restrições fisiológicas e adaptação à variação de contrastes entre objetos e o ambiente. O escurecimento mais rápido da cor do corpo é favorecido em ambientes que mostram maiores quantidades de contraste entre objetos comuns e o fundo predominante. Tipos de solo em igarapés da floresta amazônica criam ambientes distintos em relação à quantidade de contraste, resultado da quantidade de areia e argila, que oferece diferentes contrastes contra folhiço submerso. Nós investigamos as diferenças nas taxas de mudança de cor entre populações do tetra-colibri Crenuchus spilurus que representam linhagens que vivem em regiões de diferentes tipos de solo. Populações inseridas em águas pretas (solo arenoso) apresentaram maiores taxas de escurecimento da cor em resposta à exposição ao ambiente escuro de folhiço submerso. Nós propomos que a seleção natural decorrente da predação pode favorecer uma taxa de mudança de cor mais rápida em ambientes onde há maior variabilidade de contrastes entre o folhiço submerso e o solo, o que é comum na maioria dos igarapés de águas pretas.

Does soil color affect fish evolution? Differences in color change rate between lineages of the sailfin tetra

Several organisms match their skin color to the prevalent background color, granting crypsis against predators. The rate at which body color changes occur varies among organisms as a result of physiological constraints and adaptation to variation in contrasts between objects and the environmental background. Faster darkening of body color is favored in environments that show higher amounts of contrast between common objects and the prevailing background. Soil types in Amazon forest streams (igarapés) create distinct environments with respect to the amount of contrast, a result of the amount of sand and clay, which offers different contrasts against dead leaves. Here, we investigated differences in the rates of color change among populations of the sailfin tetra (Crenuchus spilurus) that represent lineages that live in regions of different soil types. Populations inserted into blackwaters (sandy soil) showed higher rates of color darkening in response to exposure to a dark environment composed by dead leaves. We propose that natural selection stemming from predation can favor faster color change rate in environments where there is higher variability of contrasts between leaf litter and soil, which is common in most blackwater streams.(AU)

Diversos organismos combinam sua coloração corporal com a cor de fundo predominante no ambiente, conferindo cripticidade contra predadores. A taxa na qual as mudanças de coloração corpórea ocorrem varia entre os organismos como resultado de restrições fisiológicas e adaptação à variação de contrastes entre objetos e o ambiente. O escurecimento mais rápido da cor do corpo é favorecido em ambientes que mostram maiores quantidades de contraste entre objetos comuns e o fundo predominante. Tipos de solo em igarapés da floresta amazônica criam ambientes distintos em relação à quantidade de contraste, resultado da quantidade de areia e argila, que oferece diferentes contrastes contra folhiço submerso. Nós investigamos as diferenças nas taxas de mudança de cor entre populações do tetra-colibri Crenuchus spilurus que representam linhagens que vivem em regiões de diferentes tipos de solo. Populações inseridas em águas pretas (solo arenoso) apresentaram maiores taxas de escurecimento da cor em resposta à exposição ao ambiente escuro de folhiço submerso. Nós propomos que a seleção natural decorrente da predação pode favorecer uma taxa de mudança de cor mais rápida em ambientes onde há maior variabilidade de contrastes entre o folhiço submerso e o solo, o que é comum na maioria dos igarapés de águas pretas.(AU)

Trade-offs direct the evolution of coloration in Galápagos land snails.

Increasingly, multiple selective factors are recognized as jointly contributing to the evolution of morphology. What is not clear is how these forces vary across communities to promote morphological diversification among related species. In this study of Galápagos endemic snails (genus Naesiotus), we test several hypotheses of colour evolution. We observe mockingbirds (genus Mimus) predating live snails and find that avian predation selects against conspicuous shells. The evolutionary outcome of this selection is a diversity of shell colours across snails of the archipelago, each closely matching local backgrounds. We also find that snails more regularly exposed to the hot, equatorial sun reflect more light than shells of species from shadier habitats, suggesting a role for thermoregulatory constraints directing colour evolution. The signature of thermoregulatory selection is most clear in comparatively young communities (on the youngest islands), while the signature of selection from predators is most evident in older communities (on the older islands). Together, our findings point to a scenario of shifting selective forces along island ontogeny and community maturity that lead to the distribution of snail coloration we observe in Galápagos. Complex selective regimes such as these may have more responsibility for morphological diversity than is currently recognized.

Ephemeral-habitat colonization and neotropical species richness of Caenorhabditis nematodes.

BACKGROUND: The drivers of species co-existence in local communities are especially enigmatic for assemblages of morphologically cryptic species. Here we characterize the colonization dynamics and abundance of nine species of Caenorhabditis nematodes in neotropical French Guiana, the most speciose known assemblage of this genus, with resource use overlap and notoriously similar external morphology despite deep genomic divergence. METHODS: To characterize the dynamics and specificity of colonization and exploitation of ephemeral resource patches, we conducted manipulative field experiments and the largest sampling effort to date for Caenorhabditis outside of Europe. This effort provides the first in-depth quantitative analysis of substrate specificity for Caenorhabditis in natural, unperturbed habitats. RESULTS: We amassed a total of 626 strain isolates from nine species of Caenorhabditis among 2865 substrate samples. With the two new species described here (C. astrocarya and C. dolens), we estimate that our sampling procedures will discover few additional species of these microbivorous animals in this tropical rainforest system. We demonstrate experimentally that the two most prevalent species (C. nouraguensis and C. tropicalis) rapidly colonize fresh resource patches, whereas at least one rarer species shows specialist micro-habitat fidelity. CONCLUSION: Despite the potential to colonize rapidly, these ephemeral patchy resources of rotting fruits and flowers are likely to often remain uncolonized by Caenorhabditis prior to their complete decay, implying dispersal-limited resource exploitation. We hypothesize that a combination of rapid colonization, high ephemerality of resource patches, and species heterogeneity in degree of specialization on micro-habitats and life histories enables a dynamic co-existence of so many morphologically cryptic species of Caenorhabditis.

Both Palatable and Unpalatable Butterflies Use Bright Colors to Signal Difficulty of Capture to Predators.

Birds are able to recognize and learn to avoid attacking unpalatable, chemically defended butterflies after unpleasant experiences with them. It has also been suggested that birds learn to avoid prey that are efficient at escaping. This, however, remains poorly documented. Here, we argue that butterflies may utilize a variety of escape tactics against insectivorous birds and review evidence that birds avoid attacking butterflies that are hard to catch. We suggest that signaling difficulty of capture to predators is a widespread phenomenon in butterflies, and this ability may not be limited to palatable butterflies. The possibility that both palatable and unpalatable species signal difficulty of capture has not been fully explored, but helps explain the existence of aposematic coloration and escape mimicry in butterflies lacking defensive chemicals. This possibility may also change the role that putative Müllerian and Batesian mimics play in a variety of classical mimicry rings, thus opening new perspectives in the evolution of mimicry in butterflies.

Keeping the band together: evidence for false boundary disruptive coloration in a butterfly.

There is a recent surge of evidence supporting disruptive coloration, in which patterns break up the animal's outline through false edges or boundaries, increasing survival in animals by reducing predator detection and/or preventing recognition. Although research has demonstrated that false edges are successful for reducing predation of prey, research into the role of internal false boundaries (i.e. stripes and bands) in reducing predation remains warranted. Many animals have stripes and bands that may function disruptively. Here, we test the possible disruptive function of wing band patterning in a butterfly, Anartia fatima, using artificial paper and plasticine models in Panama. We manipulated the band so that one model type had the band shifted to the wing margin (nondisruptive treatment) and another model had a discontinuous band located on the wing margin (discontinuous edge treatment). We kept the natural wing pattern to represent the false boundary treatment. Across all treatment groups, we standardized the area of colour and used avian visual models to confirm a match between manipulated and natural wing colours. False boundary models had higher survival than either the discontinuous edge model or the nondisruptive model. There was no survival difference between the discontinuous edge model and the nondisruptive model. Our results demonstrate the importance of wing bands in reducing predation on butterflies and show that markings set in from the wing margin can reduce predation more effectively than marginal bands and discontinuous marginal patterns. This study demonstrates an adaptive benefit of having stripes and bands.

Dynamic camouflage by Nassau groupers Epinephelus striatus on a Caribbean coral reef.

This field study describes the camouflage pattern repertoire, associated behaviours and speed of pattern change of Nassau groupers Epinephelus striatus at Little Cayman Island, British West Indies. Three basic camouflaged body patterns were observed under natural conditions and characterized quantitatively. The mean speed of pattern change across the entire body was 4.44 s (range = 0.97-9.87 s); the fastest pattern change as well as contrast change within a fixed pattern occurred within 1 s. Aside from apparent defensive camouflage, E. striatus used camouflage offensively to approach crustacean or fish prey, and three successful predation events were recorded. Although animal camouflage is a widespread tactic, dynamic camouflage is relatively uncommon and has been studied rarely in marine teleosts under natural conditions. The rapid changes observed in E. striatus suggest direct neural control of some skin colouration elements, and comparative studies of functional morphology and behaviour of colour change in other coral-reef teleosts are likely to reveal new mechanisms and adaptations of dynamic colouration.

Coarse dark patterning functionally constrains adaptive shifts from aposematism to crypsis in strawberry poison frogs.

Ecological specialization often requires tight coevolution of several traits, which may constrain future evolutionary pathways and make species more prone to extinction. Aposematism and crypsis represent two specialized adaptations to avoid predation. We tested whether the combined effects of color and pattern on prey conspicuousness functionally constrain or facilitate shifts between these two adaptations. We combined data from 17 natural populations of strawberry poison frogs, Oophaga pumilio with an experimental approach using digitalized images of frogs and chickens as predators. We show that bright coloration often co-occurs with coarse patterning among the natural populations. Dull green frogs with coarse patterning are rare in nature but in the experiment they were as easily detected as bright red frogs suggesting that this trait combination represents a transient evolutionary state toward aposematism. Hence, a gain of either bright color or coarse patterning leads to conspicuousness, but a transition back to crypsis would be functionally constrained in populations with both bright color and coarse patterning by requiring simultaneous changes in two traits. Thus, populations (or species) signaling aposematism by conspicuous color should be less likely to face an evolutionary dead end and more likely to radiate than populations with both conspicuous color and coarse patterning.

Selection of perching site background color by Hamadryas feronia (Lepidoptera: Nymphalidae) in Costa Rica: Implications for industrial melanism

Observations of the increased frequency of melanic forms in moths of the genus Biston in Great Britain after the industrial revolution lead to the development of the theory of industrial Melanism. Nonetheless, arguments against that interpretation of the experimental evidence have polarized acceptance of the concept. New evidence based on diurnal butterflies is more credible because it involves behavior that can be seen in action, during daylight, and because the natural history of the selected species is well known. An experiment was carried out in which three substrate colors (white, black, and gray) were employed to test the landing preferences of Hamadryas feronia. A marked preference was observed for landing on white and gray, and a chi-square (N=644 tests) showed evidence of a preference by males to land on white, and for females to land on gray. Black was rejected perhaps because it provides very little background matching with the butterfly’s colors. The butterfly habit of perching selectively on particular color substrates is a genetically fixed behavior, where the males possibly choose white as a tactic to be noticed by females and attract them, whereas females prefer gray to enhance crypsis and avoid attracting predators.

Observaciones en el incremento de la frecuencia de las formas melánicas de la polilla Biston de Gran Bretaña después de la revolución industrial, llevó al desarrollo de la teoría del melanismo industrial. Sin embargo, se originaron argumentos en contra de la interpretación experimental de dicho fenómeno que llevaron a polarizar su aceptación general. Nueva evidencia basada en mariposas diurnas genera nuevas perspectivas puesto que incluye el comportamiento, que puede ser apreciado durante el día. Además, la especie seleccionada es bien conocida desde el punto de vista de su historia natural. El experimento que desarrolle consiste en tres sustratos de diferente color (blanco, negro y gris) en donde se pone a prueba la preferencia de Hamadryas feronia para posarse. Se encontró una marcada tendencia a posarse sobre el blanco y el gris, chi-cuadrado (N=644), donde los machos prefirieron el blanco y las hembras el gris. El negro fue rechazado probablemente porque ofrece muy poca defensa visual al disminuir el efecto de la coloración críptica de esta especie. El habito por parte de esta mariposa de posarse selectivamente sobre sustratos de distinto color esta fijado genéticamente, los machos posiblemente prefieren blanco como una táctica para atraer hembras y las hembras prefieren gris para aumentar el efecto de su coloración críptica y así evitar ser detectadas por los depredadores.

Sequence variation in the melanocortin-1 receptor (MC1R) pigmentation gene and its role in the cryptic coloration of two South American sand lizards.

In reptiles, dorsal body darkness often varies with substrate color or temperature environment, and is generally presumed to be an adaptation for crypsis or thermoregulation. However, the genetic basis of pigmentation is poorly known in this group. In this study we analyzed the coding region of the melanocortin-1-receptor (MC1R) gene, and therefore its role underlying the dorsal color variation in two sympatric species of sand lizards (Liolaemus) that inhabit the southeastern coast of South America: L. occipitalis and L. arambarensis. The first is light-colored and occupies aeolic pale sand dunes, while the second is brownish and lives in a darker sandy habitat. We sequenced 630 base pairs of MC1R in both species. In total, 12 nucleotide polymorphisms were observed, and four amino acid replacement sites, but none of them could be associated with a color pattern. Comparative analysis indicated that these taxa are monomorphic for amino acid sites that were previously identified as functionally important in other reptiles. Thus, our results indicate that MC1R is not involved in the pigmentation pattern observed in Liolaemus lizards. Therefore, structural differences in other genes, such as ASIP, or variation in regulatory regions of MC1R may be responsible for this variation. Alternatively, the phenotypic differences observed might be a consequence of non-genetic factors, such as thermoregulatory mechanisms.

Sequence variation in the melanocortin-1 receptor (MC1R) pigmentation gene and its role in the cryptic coloration of two South American sand lizards

In reptiles, dorsal body darkness often varies with substrate color or temperature environment, and is generally presumed to be an adaptation for crypsis or thermoregulation. However, the genetic basis of pigmentation is poorly known in this group. In this study we analyzed the coding region of the melanocortin-1-receptor (MC1R) gene, and therefore its role underlying the dorsal color variation in two sympatric species of sand lizards (Liolaemus) that inhabit the southeastern coast of South America: L. occipitalis and L. arambarensis. The first is light-colored and occupies aeolic pale sand dunes, while the second is brownish and lives in a darker sandy habitat. We sequenced 630 base pairs of MC1R in both species. In total, 12 nucleotide polymorphisms were observed, and four amino acid replacement sites, but none of them could be associated with a color pattern. Comparative analysis indicated that these taxa are monomorphic for amino acid sites that were previously identified as functionally important in other reptiles. Thus, our results indicate that MC1R is not involved in the pigmentation pattern observed in Liolaemus lizards. Therefore, structural differences in other genes, such as ASIP, or variation in regulatory regions of MC1R may be responsible for this variation. Alternatively, the phenotypic differences observed might be a consequence of non-genetic factors, such as thermoregulatory mechanisms.

Fallen leaves on the water-bed: diurnal camouflage of three night active fish species in an Amazonian streamlet

Resemblance to dead leaves is a well known type of camouflage recorded for several small vertebrates that dwell in the leaf and root litter on the ground. We present here instances of such resemblance in three species of nocturnal fishes (Siluriformes and Gymnotiformes) that spend the daytime among submersed root-tangle with leaf litter in Amazonian streams. All three species are very difficult to spot visually, due both to their shape and colors which blend with the substrate, as well as to the heterogeneous nature of their cover. Two species were recorded to lie on their sides, which adds to their resemblance to dead leaves. When disturbed, one species may drift like a waterlogged leaf, whereas another moves upwards the root-tangle, exposing its fore body above the water surface. We regard their leaf-like shapes, cryptic colors, and escape movements as a convergence in defensive responses to visually hunting aquatic vertebrates, most likely diurnal predaceous fishes.

Semelhança com folhas mortas é um tipo bem conhecido de camuflagem, presente em diversos pequenos vertebrados que vivem em meio à serapilheira do chão da floresta. Apresentamos aqui exemplos deste tipo de semelhança em três espécies de peixes de hábitos noturnos (Siluriformes e Gymnotiformes) que permanecem durante o dia em meio a aglomerados de raízes e folhas submersas em igarapés amazônicos. As três espécies são difíceis de localizar visualmente, tanto devido ao formato e cores, que se confundem com o substrato, como pela heterogeneidade estrutural dos seus abrigos. Duas espécies foram observadas deitadas de lado durante o dia, o que aumenta sua semelhança com folhas mortas. Quando perturbada, uma das espécies deixa-se levar à deriva como uma folha semi-encharcada, ao passo que outra espécie se desloca para cima, nos aglomerados de raízes, expondo a porção anterior do corpo acima da superfície da água. Consideramos o formato semelhante a uma folha, as cores crípticas e os movimentos de fuga, como uma convergência de respostas defensivas a vertebrados aquáticos que caçam visualmente orientados, provavelmente peixes predadores de hábitos diurnos.

Fallen leaves on the water-bed: diurnal camouflage of three night active fish species in an Amazonian streamlet

Resemblance to dead leaves is a well known type of camouflage recorded for several small vertebrates that dwell in the leaf and root litter on the ground. We present here instances of such resemblance in three species of nocturnal fishes (Siluriformes and Gymnotiformes) that spend the daytime among submersed root-tangle with leaf litter in Amazonian streams. All three species are very difficult to spot visually, due both to their shape and colors which blend with the substrate, as well as to the heterogeneous nature of their cover. Two species were recorded to lie on their sides, which adds to their resemblance to dead leaves. When disturbed, one species may drift like a waterlogged leaf, whereas another moves upwards the root-tangle, exposing its fore body above the water surface. We regard their leaf-like shapes, cryptic colors, and escape movements as a convergence in defensive responses to visually hunting aquatic vertebrates, most likely diurnal predaceous fishes.

Semelhança com folhas mortas é um tipo bem conhecido de camuflagem, presente em diversos pequenos vertebrados que vivem em meio à serapilheira do chão da floresta. Apresentamos aqui exemplos deste tipo de semelhança em três espécies de peixes de hábitos noturnos (Siluriformes e Gymnotiformes) que permanecem durante o dia em meio a aglomerados de raízes e folhas submersas em igarapés amazônicos. As três espécies são difíceis de localizar visualmente, tanto devido ao formato e cores, que se confundem com o substrato, como pela heterogeneidade estrutural dos seus abrigos. Duas espécies foram observadas deitadas de lado durante o dia, o que aumenta sua semelhança com folhas mortas. Quando perturbada, uma das espécies deixa-se levar à deriva como uma folha semi-encharcada, ao passo que outra espécie se desloca para cima, nos aglomerados de raízes, expondo a porção anterior do corpo acima da superfície da água. Consideramos o formato semelhante a uma folha, as cores crípticas e os movimentos de fuga, como uma convergência de respostas defensivas a vertebrados aquáticos que caçam visualmente orientados, provavelmente peixes predadores de hábitos diurnos.