Nuptial Coloration Research Articles

Allopatric speciation in the desert: diversification of cichlids at their geographical and ecological range limit in Iran

Cichlids are textbook examples for rapid diversification and high species diversity. While in South America, several hundred and in Africa, more than 1500 species of cichlid fish have been described, only one single cichlid species, Iranocichla hormuzensis Coad 1982, was known from Iran, the easternmost range margin of the species-rich African cichlids (Cichlidae: Pseudocrenilabrinae). The aim of our paper was to assess the genetic and phenotypic diversity among populations of Iranocichla across most of its geographical range in Southern Iran. For this, we sequenced two mitochondrial genes and collected color observation of male nuptial coloration in different habitats. Besides conspicuous differences in male nuptial coloration, we found considerable genetic differentiation among Iranocichla populations pointing to the existence of at least two allopatric species, with no evidence of more than one species at one site. Diversification within Iranocichla started, based on our data, in the middle or late Pleistocene and was followed by further population differentiation and bottlenecks during isolation events in the last glacial maximum. Population dispersal leading to the population structure observed today most likely occurred in the course of the early Holocene sea-level rise.

Structural- and carotenoid-based throat colour patches in males of Lacerta schreiberi reflect different parasitic diseases

Host species in populations under strong pressures from parasitic diseases may evolve ornaments to signal individual host quality to conspecifics. Colour ornaments in lizards result from the interaction of different layers in the skin. When inner layers of melanin and well-arranged iridophores are combined, UV-blue structural colouration results. On the other hand, when layers of erythrophores are densely loaded with carotenoids, a UV-yellow colouration is seen. The expression of carotenoid-based traits has been frequently studied in relation to parasite infections. However, few studies have explored the relationship between parasitic diseases and structural colouration. In this study, we investigated the expression of UV-blue and UV-yellow throat colour patches in males of Lacerta schreiberi in relation to infection by haemoparasites, ixodid ticks and intestinal nematodes. The brightness of the UV-yellow throat patch (a carotenoid-based ornament) was positively correlated with body condition and negatively correlated with the number of attached ticks, supporting Hamilton and Zuk’s hypothesis. Additionally, individuals that passed nematode eggs in the faeces had UV-yellow throat patches with higher hue values (more greenish colouration). Strikingly, the individuals infected by haemoparasites of the genus Schellackia showed UV-blue throat patches (a melanin-based ornament) with higher values of both UV-blue chroma and hue (i.e., UV-biased throats) than did uninfected individuals, suggesting a key role for melanin in the nuptial colouration of this lizard species. Thus, the combined information from both UV-blue and UV-yellow throat patches may convey integrative information about individual quality in this lacertid species.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour.

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment-dependent sexual selection has played an important role. Here, we describe a very young (~90years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment-dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Intruder colour and light environment jointly determine how nesting male stickleback respond to simulated territorial intrusions.

Variation in male nuptial colour signals might be maintained by negative frequency-dependent selection. This can occur if males are more aggressive towards rivals with locally common colour phenotypes. To test this hypothesis, we introduced red or melanic three-dimensional printed-model males into the territories of nesting male stickleback from two optically distinct lakes with different coloured residents. Red-throated models were attacked more in the population with red males, while melanic models were attacked more in the melanic male lake. Aggression against red versus melanic models also varied across a depth gradient within each lake, implying that the local light environment also modulated the strength of negative frequency dependence acting on male nuptial colour.

Unsociable juvenile male three-spined sticklebacks grow more attractive

An animal’s personality may be an adaptive behavioral response of individuals to consistent differences in physiology and life-history. Studying the relationship between behavior and other fitness-related traits within the pace-of-life syndrome (POLS) framework, which explains the integration of different traits using the concept of a fast-slow life-history continuum, may thus be a useful approach to understanding the evolution and maintenance of animal personality. According to the POLS hypothesis, for example, fast individuals should be behaviorally more active, bolder or less sociable, and potentially invest more in reproduction than slow individuals. Here, we examined whether the sociability of juvenile sticklebacks (Gasterosteus aculeatus) is linked with their key reproductive traits, carotenoid-based nuptial coloration of males and egg production of females. We also tested whether experimental manipulation of environmental conditions (control vs. warm winter) can change pace-of-life and the link between behavioral and reproductive traits. Male sticklebacks prone to shoaling expressed lower peak red coloration at the reproductive stage, during which they were solitary and territorial. In females, fecundity was not correlated with early social behavior. Experimental sticklebacks reared in warm winter conditions decreased their investment in reproduction, but the negative relationship between sociability and sexual signal of males was maintained. Our results suggest that the POLS could partly explain the maintenance of personality under predation pressure or severe mating competition. In natural environments, any benefit to sociable male sticklebacks may be counterbalanced by the cost of growing less attractive. Why do animals vary in personality, and how is such variation maintained within a population? An interesting approach for understanding this is studying how personality traits are correlated with other fitness-related traits within the pace-of-life framework. For the first time, our results show the link between sociability at the juvenile stage and the expression of sexual ornament during reproduction in male three-spined sticklebacks. Sociable juveniles may benefit from reduced predation risk, but they grow less attractive and this may reduce their mating success during reproduction. Thus, the trade-off between survival and reproduction may contribute to the maintenance of among-individual variation in behavior.

The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae).

Closely related animal lineages often vary in male coloration, and ecological selection is hypothesized to shape this variation. The role of ecological selection in inhibiting male color has been documented extensively at the population level, but relatively few studies have investigated the evolution of male coloration across a clade of closely related species. Darters are a diverse group of fishes that vary in the presence of elaborate male nuptial coloration, with some species exhibiting vivid color patterns and others mostly or entirely achromatic. We used phylogenetic logistic regression to test for correlations between the presence/absence of color traits across darter species and the ecological conditions in which these species occur. Environmental variables were correlated with the presence of nuptial color in darters with colorful species tending to inhabit environments that would support fewer predators and potentially transmit a broader spectrum of natural light compared to species lacking male coloration. We also tested the color preferences of a common darter predator, largemouth bass, and found that it exhibits a strong preference for red, providing further evidence of predation as a source of selection on color evolution in darters. Ecological selection therefore appears to be an important factor in dictating the presence or absence of male coloration in this group of fishes.

Space Use Strategies and Nuptial Color in European Green Lizards

Abstract The conspicuous colors found in many lizards transfer information about their owner’s characteristics that are relevant to mating and social systems. Female European Green Lizards (Lacerta viridis) have been shown to prefer males with high ultraviolet (UV) throat reflectance. Additionally, components of throat patch color (such as UV chroma and brightness) have been shown to be condition-dependent and to signal relative head size and health status. In this study, we investigated whether or not different components of male nuptial color and other relevant traits were associated with characteristics of male space use during the reproductive season at two different locations. In Site 1, lizard density was two times higher, territory size was one third as large, and spatial overlap between territories was about half as large as in Site 2. Males at Site 1 showed movement patterns consistent with a mix of territorial and floater individuals, with floaters exhibiting greater throat brightness. Those mal...

Genetic conflict between sexual signalling and juvenile survival in the three-spined stickleback.

BackgroundSecondary sexual traits and mating preferences may evolve in part because the offspring of attractive males inherit attractiveness and other genetically correlated traits such as fecundity and viability. A problem regarding these indirect genetic mechanisms is how sufficient genetic variation in the traits subject to sexual selection is maintained within a population. Here we explored the additive genetic correlations between carotenoid-based male ornament colouration, female fecundity and juvenile survival rate in the three-spined stickleback (Gasterosteus aculeatus) to test the possibility that attractiveness genes reduce important fitness components in the bearers not expressing the sexual trait.ResultsMale sexual attractiveness (i.e., red nuptial colouration) as well as female fecundity and juvenile viability showed heritable variations in the three-spined stickleback. Thus, females can gain indirect benefits by mating with an attractive male. There was a strong positive genetic correlation between female fecundity and juvenile viability. However, red sexual signal of male sticklebacks was negatively genetically correlated with juvenile survival, suggesting genetic conflict between attractiveness and viability. There was no significant correlation between attractiveness of brothers and fecundity of sisters, suggesting no intra-locus sexual conflict.ConclusionsThe negative effects of mating with a colourful male on offspring viability may contribute to maintaining the heritable variation under strong directional sexual selection. The strength of indirect sexual selection may be weaker than previously thought due to the hidden genetic conflicts.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0613-4) contains supplementary material, which is available to authorized users.

Correlated Evolution of Short Wavelength Sensitive Photoreceptor Sensitivity and Color Pattern in Lake Malawi Cichlids

For evolutionary ecologists, the “holy grail” of visual ecology is to establish an unambiguous link between photoreceptor sensitivity, the spectral environment, and the perception of specific visual stimuli (e.g., mates, food, predators, etc.). Due to the bright nuptial colors of the males, and the role female mate choice plays in their evolution, the haplochromine cichlid fishes of the African great lakes are favorite research subjects for such investigations. Despite this attention, current evidence is equivocal; while distinct correlations among photoreceptor sensitivity, photic environment, and male coloration exist in Lake Victorian haplochromines, attempts to find such correlations in Lake Malawian cichlids have failed. Lake Malawi haplochromines have a wide variability in their short-wavelength-sensitive photoreceptors, especially compared to their mid- and long-wavelength-sensitive photoreceptors; these cichlids also vary in the degree to which they express one of three basic color patterns (vertical bars, horizontal stripes, and solid patches of colors), each of which is likely used in a different form of communication. Thus, we hypothesize that, in these fishes, spectral sensitivity and color pattern have evolved in a correlated fashion to maximize visual communication; specifically, ultraviolet sensitivity should be found in vertically-barred species to promote ‘private’ communication, while striped species should be less likely to have ultraviolet sensitivity, since their color pattern carries ‘public’ information. Using phylogenetic independent contrasts, we found that barred species had strong sensitivity to ultraviolet wavelengths, but that striped species typically lacked sensitivity to ultraviolet light. Further, the only variable, even when environmental variables were simultaneously considered, that could predict ultraviolet sensitivity was color pattern. We also found that, using models of correlated evolution, color pattern and ultraviolet sensitivity are correlated in Lake Malawi cichlid evolution, with the likely ancestor being a vertically-barred, ultraviolet-sensitive species, the descendants of which lost both ultraviolet sensitivity and a barred color pattern. These results, indicating that communication of ‘public’ and ‘private’ signals is mediated via differing perceptions of color patterns, suggest a functional connection between visual sensitivity and colour pattern, a novel finding in Lake Malawi cichlids.

A Morphological Study ofCynops pyrrhogasterfrom the Chita Peninsula: Rediscovery of the “Extinct” Atsumi Race Endemic to Peninsular Regions of Aichi Prefecture, Central Japan

In the Japanese fire-bellied newt, Cynops pyrrhogaster, six local races were reported (Atsumi, Hiroshima, Kanto, Sasayama, Tohoku, and Intermediate) on the basis of morphological and ethological traits. Among them, the Atsumi race was reported only from a locality of the Atsumi Peninsula, Aichi Prefecture, but this race has been thought to be extinct after the 1960s. In the present study, we collected C. pyrrhogaster at a wetland of the Chita Peninsula, which is located west of the Atsumi Peninsula. The specimens resembled the Atsumi race in dorsal and ventral color pattern, absence of male nuptial color, small body size, and elongated filamentous process of tail tip. Newts from Chita differed from the Atsumi race in the tail height/tail length ratio, but this value was highly variable even among populations within another race (the Intermediate race). Judging from these results, we suggest that C. pyrrhogaster from the Chita Peninsula should be regarded as a part of the Atsumi race, which has long been thought to be extinct. Unfortunately, C. pyrrhogaster at Chita is also threatened with extinction, and immediate protection is seriously needed to prevent this enigmatic local race from complete extinction.

Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

AbstractSexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected--the red nuptial coloration of the three-spined stickleback--is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.

The origin and genetic divergence of “black” kokanee, a novel reproductive ecotype ofOncorhynchus nerka

Kokanee and sockeye salmon are the freshwater-resident and anadromous forms, respectively, of Oncorhynchus nerka. Unique populations of “black” kokanee are found in Lake Saiko, Japan, and in Anderson and Seton lakes in the southwestern interior of British Columbia. They are distinct from other populations of O. nerka in that black kokanee display black nuptial colouration and they spawn between 20 to 70 m below the surface of lakes in the winter or early spring. Analysis of mitochondrial DNA and nine microsatellite loci supported the hypothesis that black kokanee in Lake Saiko and in Anderson and Seton lakes have had a diphyletic origin resulting from at least two episodes of divergence in the North Pacific basin. Further, black kokanee in the Anderson and Seton lakes system were genetically distinct from sympatric populations of sockeye salmon in Gates and Portage creeks (inlets to Anderson and Seton lakes, respectively) and were distinct from one another. Anderson and Seton lake black kokanee differed dramatically from one another in standard length at maturity, but no differences were found between the two populations in size-adjusted maximum body depth or in gill raker numbers. Independent origins of black kokanee represent novel diversity within O. nerka, are consistent with the importance of parallel evolution in the origin of biodiversity, and suggest that independent management regimes are required for the persistence of black kokanee biodiversity within a physically interconnected lake system.

Sexual characteristics of high-temperature sterilized male Mozambique tilapia, Oreochromis mossambicus.

IntroductionIn order to clarify the effect of extremely high temperature on gonads of fish, juveniles of the Mozambique tilapia, Oreochromis mossambicus, at three days after hatching (d.a.h.) were reared at a high temperature (37 ± 0.5 °C) for 50 days. The heat-treated fish were then cultivated at a normal water temperature for over six months.ResultsThe testes of all individuals heat-treated for 50 days were sterile. Histological analysis revealed the complete absence of all stages of spermatogenic germ cells in the testes of the heat-treated males; however, structures within a layer of epithelial cells lining the efferent ducts were observed to actively secrete sperm fluid into the ducts, as in the mature testes of normal males. Clusters of cells immunopositive against P450scc and 3β-hydroxysteroid dehydrogenase were observed in the sterilized testes. Leydig cells had developed smooth endoplasmic reticulum and several mitochondria with tubular cristae indicating active steroidogenesis. The sterilized males displayed male nuptial coloration, actively dug spawning nests, and mated with normal mature females. However, females mated with these males initially brooded their eggs normally but released them prematurely at 4–5 days. All the released eggs were unfertilized and dead.ConclusionHeat-sterilized male tilapia matures endocrinologically but completely lacks spermatogenic germ cells.

Population-Specific Covariation between Immune Function and Color of Nesting Male Threespine Stickleback.

Multiple biological processes can generate sexual selection on male visual signals such as color. For example, females may prefer colorful males because those males are more readily detected (perceptual bias), or because male color conveys information about male quality and associated direct or indirect benefits to females. For example, male threespine stickleback often exhibit red throat coloration, which females prefer both because red is more visible in certain environments, and red color is correlated with male immune function and parasite load. However, not all light environments favor red nuptial coloration: more tannin-stained water tends to favor the evolution of a melanic male phenotype. Do such population differences in stickleback male color, driven by divergent light environments, lead to changes in the relationship between color and immunity? Here, we show that, within stickleback populations, multiple components of male color (brightness and hue of four body parts) are correlated with multiple immune variables (ROS production, phagocytosis rates, and lymphocyte:leukocyte ratios). Some of these color-immune associations persist across stickleback populations with very different male color patterns, whereas other color-immune associations are population-specific. Overall, lakes with red males exhibit stronger color-immune covariance while melanic male populations exhibit weak if any color-immune associations. Our finding that color-immunity relationships are labile implies that any evolution of male color traits (e.g., due to female perceptual bias in a given light environment), can alter the utility of color as an indicator of male quality.

Differentiation of visual spectra and nuptial colorations of two Paratanakia himantegus subspecies (Cyprinoidea: Acheilognathidae) in response to the distinct photic conditions of their habitats.

Vision, an important sensory modality of many animals, exhibits plasticity in that it adapts to environmental conditions to maintain its sensory efficiency. Nuptial coloration is used to attract mates and hence should be tightly coupled to vision. In Taiwan, two closely related bitterlings (Paratanakia himantegus himantegus and Paratanakia himantegus chii) with different male nuptial colorations reside in different habitats. We compared the visual spectral sensitivities of these subspecies with the ambient light spectra of their habitats to determine whether their visual abilities correspond with photic parameters and correlate with nuptial colorations. Theelectroretinogram (ERG) results revealed that the relative spectral sensitivity of P.h. himantegus was higher at 670 nm, but lower at 370 nm, than the sensitivity of P. h. chii. Both bitterlings could perceive and reflect UV light, but the UV reflection patterns differed between genders. Furthermore, the relative irradiance intensity of the light spectra in the habitat of P. h. himantegus was higher at long wavelengths (480-700 nm), but lower at short wavelengths (350-450 nm), than the light spectra in the habitats of P. h.chii. Two phylogenetically closely related bitterlings, P. h. himantegus and P. h. chii, dwell in different waters and exhibit different nuptial colorations and spectral sensitivities, which may be the results of speciation by sensory drive. Sensory ability and signal diversity accommodating photic environment may promote diversity of bitterling fishes. UV light was demonstrated to be a possible component of bitterling visual communication. The UV cue may assist bitterlings in genderidentification.

Ecological constraint and the evolution of sexual dichromatism in darters.

It is not known how environmental pressures and sexual selection interact to influence the evolution of extravagant male traits. Sexual and natural selection are often viewed as antagonistic forces shaping the evolution of visual signals, where conspicuousness is favored by sexual selection and crypsis is favored by natural selection. Although typically investigated independently, the interaction between natural and sexual selection remains poorly understood. Here, we investigate whether sexual dichromatism evolves stochastically, independent from, or in concert with habitat use in darters, a species-rich lineage of North American freshwater fish. We find the evolution of sexual dichromatism is coupled to habitat use in darter species. Comparative analyses reveal that mid-water darter lineages exhibit a narrow distribution of dichromatism trait space surrounding a low optimum, suggesting a constraint imposed on the evolution of dichromatism, potentially through predator-mediated selection. Alternatively, the transition to benthic habitats coincides with greater variability in the levels of dichromatism that surround a higher optimum, likely due to relaxation of the predator-mediated selection and heterogeneous microhabitat dependent selection regimes. These results suggest a complex interaction of sexual selection with potentially two mechanisms of natural selection, predation and sensory drive, that influence the evolution of diverse male nuptial coloration in darters.

Enneapterygius phoenicosoma, a New Species of Triplefin (Tripterygiidae) from the Western Pacific Ocean

A new species of triplefin (Tripterygiidae), Enneapterygius phoenicosoma, is described on the basis of 71 type specimens (17.2–37.2 mm standard length: SL) from southern Japan. An additional five specimens from the Caroline Islands and Vanuatu are also identified as belonging to this species. Males of the new species have the same distinct nuptial coloration as males of the Hawaiian endemic species E. atriceps (Jenkins, 1903). Comparisons of the present material with the holotype and 46 non-type specimens of E. atriceps show, however, that E. phoenicosoma differs from the latter in having a simple nasal tentacle (vs a bilobed tentacle in E. atriceps); lower counts of the anal-fin soft rays (16–18, mode 17 vs 19–21, 19); second dorsal-fin spines (11–13, 12 vs 12–15, 14); scale rows in longitudinal series (32–35, 33 vs 35–37, 36); and pored lateral-line scales (16–19, 17 vs 17–20, 19); a higher count of the pectoral-fin rays (15–17, 16 vs 14–17, 15); and several morphometric features, including the lengths of the dorsal-fin spines and rays, the second dorsal-fin base, and the anal-fin base. The new species grows larger than E. atriceps (largest recorded size, 37.2 mm SL vs 26.9 mm SL in E. atriceps).

Castration affects reproductive but not aggressive behavior in a cichlid fish

Gonads are the main source of sex steroids, which have been implicated in the regulation of sexually differentiated behavior, such as reproductive and aggressive displays. In the Mozambique tilapia (Oreochromis mossambicus) territorial males have higher androgen levels than non-territorials, express reproductive behavior and use a urine-borne pheromone to signal their social status towards conspecifics. Here we investigated the effects of gonadectomy on the circulating levels of androgens and cortisol, and on the expression of aggressive and reproductive behavior (nest building, courtship behavior, and nuptial coloration). Males were either castrated, urine bladder damaged, or sham-operated and visually exposed to a group of females during 8 consecutive days and subsequently to a male on day 9. The urine bladder damaged treatment was included in the experimental design because a full castration procedure in this species causes quite often damage to the urine bladder. Gonadectomy lowers dramatically the circulating levels of androgens measured at 4 and 8days post-castration and abolishes the expression of nest building, courtship behavior and nuptial coloration, but has no effect on the expression of aggressive behavior. These results confirm the gonads as the main source of androgens in this species and show that androgens are necessary for the expression of reproductive behaviors. However, the expression of aggressive behavior seems to be decoupled from gonadal steroids, namely androgens, suggesting the action of independent central mechanisms.

Association between parasite load and orange, but not blue, male nuptial colouration in Etheostoma caeruleum

The hypothesis that males possessing more vivid nuptial colouration are of better quality with regard to individual measures of health such as parasite infection was investigated by taking spectral measurements of orange and blue bars in the nuptial males of a sexually dichromatic stream fish rainbow darter Etheostoma caeruleum to determine if male colouration in this species varied with parasite load in the form of black spot disease. The yellow chroma of orange bars, i.e. the relative contribution of wavelengths in the range of 550-625 nm to total brightness, was the only spectral measurement significantly associated with parasite counts. These results are discussed in the context of sexual selection and the potential of orange bars in E. caeruleum to serve as honest indicators of quality to potential mates.