Nuptial Coloration Research Articles

Genomics of Parallel Ecological Speciation in Lake Victoria Cichlids.

The genetic basis of parallel evolution of similar species is of great interest in evolutionary biology. In the adaptive radiation of Lake Victoria cichlid fishes, sister species with either blue or red-back male nuptial coloration have evolved repeatedly, often associated with shallower and deeper water, respectively. One such case is blue and red-backed Pundamilia species, for which we recently showed that a young species pair may have evolved through "hybrid parallel speciation". Coalescent simulations suggested that the older species P. pundamilia (blue) and P. nyererei (red-back) admixed in the Mwanza Gulf and that new "nyererei-like" and "pundamilia-like" species evolved from the admixed population. Here, we use genome scans to study the genomic architecture of differentiation, and assess the influence of hybridization on the evolution of the younger species pair. For each of the two species pairs, we find over 300 genomic regions, widespread across the genome, which are highly differentiated. A subset of the most strongly differentiated regions of the older pair are also differentiated in the younger pair. These shared differentiated regions often show parallel allele frequency differences, consistent with the hypothesis that admixture-derived alleles were targeted by divergent selection in the hybrid population. However, two-thirds of the genomic regions that are highly differentiated between the younger species are not highly differentiated between the older species, suggesting independent evolutionary responses to selection pressures. Our analyses reveal how divergent selection on admixture-derived genetic variation can facilitate new speciation events.

Prevalence of disruptive selection predicts extent of species differentiation in Lake Victoria cichlids.

Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence of disruptive ecological selection differs between sympatric sister species that are at different stages of speciation. Some of our species pairs do (Pundamilia) and others do not (Neochromis) differ distinctively in sexually selected male nuptial coloration. We find that (i) evidence for disruptive selection, and for evolutionary response to it, is prevalent in traits that are differentiated between sister species; (ii) prevalence of both predicts the extent of genetic differentiation; and (iii) genetic differentiation is weaker in species pairs with conserved male nuptial coloration. Our results speak to the existence of two different mechanisms of speciation with gene flow: speciation mainly by sexual selection tightly followed by ecological character displacement in some cases and speciation mainly by divergent ecological selection in others.

Developmental effects of environmental light on male nuptial coloration in Lake Victoria cichlid fish.

BackgroundEfficient communication requires that signals are well transmitted and perceived in a given environment. Natural selection therefore drives the evolution of different signals in different environments. In addition, environmental heterogeneity at small spatial or temporal scales may favour phenotypic plasticity in signaling traits, as plasticity may allow rapid adjustment of signal expression to optimize transmission. In this study, we explore signal plasticity in the nuptial coloration of Lake Victoria cichlids, Pundamilia pundamilia and Pundamilia nyererei. These two species differ in male coloration, which mediates species-assortative mating. They occur in adjacent depth ranges with different light environments. Given the close proximity of their habitats, overlapping at some locations, plasticity in male coloration could contribute to male reproductive success but interfere with reproductive isolation.MethodsWe reared P. pundamilia, P. nyererei, and their hybrids under light conditions mimicking the two depth ranges in Lake Victoria. From photographs, we quantified the nuptial coloration of males, spanning the entire visible spectrum. In experiment 1, we examined developmental colour plasticity by comparing sibling males reared in each light condition. In experiment 2, we assessed colour plasticity in adulthood, by switching adult males between conditions and tracking coloration for 100 days.ResultsWe found that nuptial colour in Pundamilia did respond plastically to our light manipulations, but only in a limited hue range. Fish that were reared in light conditions mimicking the deeper habitat were significantly greener than those in conditions mimicking shallow waters. The species-specific nuptial colours (blue and red) did not change. When moved to the opposing light condition as adults, males did not change colour.DiscussionOur results show that species-specific nuptial colours, which are subject to strong divergent selection by female choice, are not plastic. We do find plasticity in green coloration, a response that may contribute to visual conspicuousness in darker, red-shifted light environments. These results suggest that light-environment-induced plasticity in male nuptial coloration in P. pundamilia and P. nyererei is limited and does not interfere with reproductive isolation.

How does male-male competition generate negative frequency-dependent selection and disruptive selection during speciation?

Natural selection has been shown to drive population differentiation and speciation. The role of sexual selection in this process is controversial; however, most of the work has centered on mate choice while the role of male–male competition in speciation is relatively understudied. Here, we outline how male–male competition can be a source of diversifying selection on male competitive phenotypes, and how this can contribute to the evolution of reproductive isolation. We highlight how negative frequency-dependent selection (advantage of rare phenotype arising from stronger male–male competition between similar male phenotypes compared with dissimilar male phenotypes) and disruptive selection (advantage of extreme phenotypes) drives the evolution of diversity in competitive traits such as weapon size, nuptial coloration, or aggressiveness. We underscore that male–male competition interacts with other life-history functions and that variable male competitive phenotypes may represent alternative adaptive options. In addition to competition for mates, aggressive interference competition for ecological resources can exert selection on competitor signals. We call for a better integration of male–male competition with ecological interference competition since both can influence the process of speciation via comparable but distinct mechanisms. Altogether, we present a more comprehensive framework for studying the role of male–male competition in speciation, and emphasize the need for better integration of insights gained from other fields studying the evolutionary, behavioral, and physiological consequences of agonistic interactions.

Female Mate Choice Based on Male Nuptial Coloration in Pale Chub,Zacco platypus

Males of many animals exhibit conspicuous secondary sexual traits, which are often the result of sexual selection. During the breeding period of the pale chub (Pisces: Cyprinidae), males show various sexual traits, such as long anal fins, breeding tubercles on the head, and/or conspicuous red and greenish-blue nuptial colorations. Although these conspicuous sexual dimorphisms and dichromatisms indicate that this can serve as a model species for understanding sexual selection, it is unclear whether these male sexual traits are related to female mate choice. This study examined the relationships between female mate choice and male sexual traits under laboratory conditions. In a dichotomous choice experiment, no relationship was found between female preference and male body size, anal fin length or number of breeding tubercles. In addition, female preference was not detected for traits related to the greenish-blue nuptial color of males. Instead, females chose males based on the degree of expression of red nuptial coloration. Such female preference may be useful for selecting high-quality males with good foraging abilities or good immune function related to carotenoids and sexual hormones. The present study suggests that red nuptial coloration of the male pale chub evolved in part through female mate choice.

Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish.

Distinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.

Do River Drainage Boundaries Coincide with Phylogeographic Breaks in the Redband Darter?

The Redband Darter, Etheostoma luteovinctum, is a benthic headwater fish species found in the Caney Fork and Stones rivers (Cumberland River) and the Duck and Elk rivers (Tennessee River) of central Tennessee. Phylogenetic analyses of 2601 amplified fragment length polymorphisms (AFLPs) were used to assess the relationships among populations and identified two genetically distinct lineages of Redband Darter. One lineage is comprised of populations in the Duck R., Elk R., Middle Fork Stones R., West Fork Stones R., and Hickory Creek of the Caney Fork River, while the other lineage is confined to the remainder of the known localities in the Cumberland R. drainage. As clades were not restricted to drainage or system boundaries, patterns suggest system and drainage transfers. Additionally, morphological variation was examined among populations using standard meristic data and nuptial male color and pigmentation characteristics. Although some morphological traits varied between the two clades, members were not clearly diagnosable using morphology. Taxonomic recognition is not proposed for the two identified clades; however, each clade should be recognized as an evolutionarily significant unit and regarded as such in future conservation efforts. Furthermore, this study demonstrates the utility of AFLPs to assess genetic variation and phylogenetic relationships for species-level taxonomic or phylogeographic studies.

Effects of energy and thermoregulation time on physiological state and sexual signal in a lizard.

Theory of sexual selection states that males often develop showy signals, which reduce their survival but increase their reproductive success. During mate choice, these conspicuous signals can be honest indicators of individual quality conveying information about the signaler's physiological state. Sexually selected signals are influenced by many environmental factors; however, whether signals and physiological state are affected together is rarely studied. The ultraviolet-blue throat color of male Lacerta viridis is an intra- and intersexually selected signal connected to blood parasite infection and influenced by environmental factors. The aim of this study was to experimentally investigate how ecologically relevant environmental factors affect color signal intensity and key physiological traits parallel. During the mating season, we exposed 40 adult male lizards infected with blood parasites to food and basking time treatments in a full factorial design. We measured color, amount of reactive oxygen metabolites (ROMs), hematocrit, immunocompetence, and blood parasite intensity before and after treatments. High basking time resulted in elevated immunocompetence coupled with increased ROMs. The high food treatment increased nuptial color brightness, but also increased ROMs and decreased immunocompetence. In summary, our study provides experimental evidence about environmentally induced parallel changes in an honest sexual signal and several quality-indicator physiological traits. We showed that available energy and time for high metabolism have independent and sometimes opposite effects on individual state.

Responses of Galápagos Lava Lizards (Microlophus bivittatus) to Manipulation of Female Nuptial Coloration on Lizard Robots

Abstract Females of some lizard species exhibit conspicuous coloration during the breeding cycle (“nuptial coloration”) that elicits male courtship. We conducted two field experiments with San Cristobal Lava Lizards (Microlophus bivittatus) in the Galapagos Islands to determine how the presence and extent of nuptial coloration on lizard robots affected responses of adult males and females. Robots programmed to perform conspecific bobbing displays had a morphological appearance that mimicked (1) a conspecific female without nuptial coloration (non-red control stimulus); (2) a conspecific female with nuptial coloration (normal red stimulus); or (3) a female with an extent of nuptial coloration beyond the range of conspecific variation (super-normal red stimulus). In Experiment 1, subjects witnessed two stimuli in sequence, being presented first with the side of a robot that exhibited conspecific nuptial coloration or with the opposite side of the same robot that lacked nuptial coloration. Results showed no ...

Darter (Percidae: Etheostoma) species differ in their response to video stimuli

Video playback experiments offer unique opportunities for behavioural tests due to the breadth and ease of possible manipulations available to stimuli. However, serious limitations to video playback experiments exist, primarily the need to configure a technology designed for human vision to replicate stimuli for a nonhuman viewer. Here, we test the effectiveness of video playback for two species of freshwater fish, Etheostoma barrenense and Etheostoma zonale . The focal species are closely related sympatric species that have distinct male nuptial coloration. Dichotomous choice assays using video stimuli showed that female E. zonale prefer video of conspecific males whereas female E. barrenense showed no preference for videos of conspecific or heterospecific males. Comparisons of video trials to live trials indicate that response to video playback is comparable to responses to live stimuli in female E. zonale but not in female E. barrenense . Differences in monitor replication of species-specific coloration may account for the asymmetry in response, and future work should further test colour-based recognition of video stimuli in E. zonale .

Visual adaptation in Lake Victoria cichlid fishes: depth-related variation of color and scotopic opsins in species from sand/mud bottoms

BackgroundFor Lake Victoria cichlid species inhabiting rocky substrates with differing light regimes, it has been proposed that adaptation of the long-wavelength-sensitive (LWS) opsin gene triggered speciation by sensory drive through color signal divergence. The extensive and continuous sand/mud substrates are also species-rich, and a correlation between male nuptial coloration and the absorption of LWS pigments has been reported. However, the factors driving genetic and functional diversity of LWS pigments in sand/mud habitats are still unresolved.ResultsTo address this issue, nucleotide sequences of eight opsin genes were compared in ten Lake Victoria cichlid species collected from sand/mud bottoms. Among eight opsins, the LWS and rod-opsin (RH1) alleles were diversified and one particular allele was dominant or fixed in each species. Natural selection has acted on and fixed LWS alleles in each species. The functions of LWS and RH1 alleles were measured by absorption of reconstituted A1- and A2-derived visual pigments. The absorption of pigments from RH1 alleles most common in deep water were largely shifted toward red, whereas those of LWS alleles were largely shifted toward blue in both A1 and A2 pigments. In both RH1 and LWS pigments, A2-derived pigments were closer to the dominant light in deep water, suggesting the possibility of the adaptation of A2-derived pigments to depth-dependent light regimes.ConclusionsThe RH1 and LWS sequences may be diversified for adaptation of A2-derived pigments to different light environments in sand/mud substrates. Diversification of the LWS alleles may have originally taken place in riverine environments, with a new mutation occurring subsequently in Lake Victoria.

A New Species of Labeotropheus (Perciformes: Cichlidae) from Southern Lake Malaŵi, Africa

Labeotropheus is a genus of haplochromine cichlids endemic to Lake Malaŵi, Africa. Since its original description, surprisingly few additional species have been described, largely due to a misinterpretation of the historical taxonomic treatment of allopatric populations of Labeotropheus. Previously published evidence of genetic and morphological divergence among southern populations of Labeotropheus suggests that species diversity is underestimated. Morphometric, meristic, and color characteristics are employed to describe a new species of Labeotgropheus endemic to Mumbo Island and Thumbi West Island near the Nankumba Peninsula in southern Lake Malaŵi. The new species is distinguished from congeners by a wider body, longer pectoral fins, a shorter snout, and male nuptial coloration.

Phenotypic plasticity drives a depth gradient in male conspicuousness in threespine stickleback, Gasterosteus aculeatus.

Signal evolution is thought to depend on both a signal's detectability or conspicuousness (signal design) as well as any extractable information it may convey to a potential receiver (signal content). While theoretical and empirical work in sexual selection has largely focused on signal content, there has been a steady accrual of evidence that signal design is also important for trait evolution. Despite this, relatively little attention has been paid to spatial variation in the conspicuousness of a given signal, especially over small spatial scales (relative to an organism's dispersal distance). Here, we show that visual signals of male threespine stickleback vary in conspicuousness, depending on a male's nest depth within a given lake. Deeper nesting males were typically more chromatically conspicuous than shallow nesting males. This trend is partly because all male stickleback are more conspicuous in deep optical environments. However, deep males are even more conspicuous than environmentally driven null expectations, while shallow males tend to be disproportionally cryptic. Experimental manipulation of male nesting depth induced plastic changes in nuptial color that replicated the natural gradients in conspicuousness. We discuss a number of potential mechanisms that could produce depth gradients in conspicuousness in male stickleback, including concomitant depth gradients in diet, predation pressure, male/female density, female preference, and opportunity for sexual selection.

Transcriptional mechanisms underlying life-history responses to climate change in the three-spined stickleback.

Phenotypic plasticity, the ability of an organism to express different phenotypes depending on the environment, provides an important mechanism by which an animal population can persist under rapid climate change. We experimentally tested both life‐history and transcriptional responses of an ecological model species, the three‐spined stickleback, to warm acclimation at the southern edge of its European range. We explored cross‐environment genetic correlations of key life‐history traits in male sticklebacks exposed to long‐term temperature changes to examine whether the plasticity pattern was variable among genotypes by using a character‐state approach. We also studied gene expression plasticity by analysing both whole‐transcriptome and candidate gene expression in brain and liver. Male sticklebacks that developed under warmer conditions during winter were smaller in size and invested less in nuptial coloration at the beginning of the breeding season, showing similar responses across different genotypes. The lack of genetic variation in life‐history responses may limit any future evolution of the thermal reaction norm in the study population. After long‐term exposure to increased winter temperatures, genes responsible for several metabolic and oxidation–reduction processes were upregulated, and some hormone genes involved in growth and reproduction were downregulated in the brain. In the liver, there was no significantly represented gene ontology by the differentially expressed genes. Since a higher temperature leads to a higher resting metabolic rate, living in warmer environments may incur higher energetic costs for ectotherms to maintain cellular homoeostasis, resulting in negative consequences for life‐history traits. The expression of genes related to metabolism, cellular homoeostasis and regulatory signalling may underlie temperature‐induced changes in life history.

Web image search revealed large-scale variations in breeding season and nuptial coloration in a mutually ornamented fish, Tribolodon hakonensis

Geographic variations in reproductive traits are important for evolutionary biology, but often difficult to investigate because of the need for a large-scale survey and the ephemeral nature of secondary sexual characteristics. Here, using web image searches (Google Images and Twitter), we revealed large-scale geographic variations (>1500 km) in breeding timing and nuptial coloration in the mutually ornamented fish, Japanese dace (Tribolodon hakonensis). As this fish is easily caught and many anglers upload their photographs on the web, we were able to find a total of 401 high-resolution photographs from all over Japan. Breeding periods were determined from dates of photographs with/without nuptial coloration, which matched with previous studies. We also found that breeding periods might have advanced three weeks over the last 80 years in the Chitose River, potentially because of climate change. Additionally, the pattern of latitudinal cline for breeding timing revealed delayed timing in higher latitudes, although regional variations were also high. Finally, we quantified the patterns of nuptial coloration for this mutually ornamented fish, and confirmed that over 80% of individuals showed typical colorations, but others showed rare phenotypes that were never previously described, including an intermediate coloration between T. hakonensis and a potentially hybridizing species, T. brandtii. Our web-based method for estimating breeding phenology could be adopted for organisms with temporal sexual characteristics, such as plants (e.g., flowering time) and some fishes. Web image analyses are still preliminarily with many limitations, but could be promising for investigating variations in visible traits.

A compendium of developmental gene expression in Lake Malawi cichlid fishes

BackgroundLake Malawi cichlids represent one of a growing number of vertebrate models used to uncover the genetic and developmental basis of trait diversity. Rapid evolutionary radiation has resulted in species that share similar genomes but differ markedly in phenotypes including brains and behavior, nuptial coloration and the craniofacial skeleton. Research has begun to identify the genes, as well as the molecular and developmental pathways that underlie trait divergence.ResultsWe assemble a compendium of gene expression for Lake Malawi cichlids, across pharyngula (the phylotypic stage) and larval stages of development, encompassing hundreds of gene transcripts. We chart patterns of expression in Bone morphogenetic protein (BMP), Fibroblast growth factor (FGF), Hedgehog (Hh), Notch and Wingless (Wnt) signaling pathways, as well as genes involved in neurogenesis, calcium and endocrine signaling, stem cell biology, and numerous homeobox (Hox) factors—in three planes using whole-mount in situ hybridization. Because of low sequence divergence across the Malawi cichlid assemblage, the probes we employ are broadly applicable in hundreds of species. We tabulate gene expression across general tissue domains, and highlight examples of unexpected expression patterns.ConclusionsOn the heels of recently published genomes, this compendium of developmental gene expression in Lake Malawi cichlids provides a valuable resource for those interested in the relationship between evolution and development.

The evolution of male nuptial colour in a sexually dimorphic group of fishes (Percidae: Etheostomatinae).

To test hypotheses explaining variation in elaborate male colouration across closely related species groups, ancestral-state reconstructions and tests of phylogenetic signal and correlated evolution were used to examine the evolution of male body and fin colouration in a group of sexually dichromatic stream fishes known as darters (Percidae: Etheostomatinae). The presence or absence of red-orange and blue-green male colour traits were scored across six body regions in 99 darter species using a recently estimated amplified fragment length polymorphism (AFLP) phylogeny for comparative analyses. Ancestral-state reconstructions infer the most recent common ancestor of darters to lack red-orange colour and possess blue-green colour on different body regions, suggesting variation between species is due to independent gains of red-orange and losses of blue-green. Colour traits exhibit substantial phylogenetic signal and are highly correlated across body regions. Comparative analyses were repeated using an alternative phylogenetic hypothesis based on one mitochondrial and two nuclear genes, yielding similar results to analyses based on the AFLP phylogeny. Red-orange colouration in darters appears to be derived; whereas, blue-green appears to be ancestral, which suggests that different selection mechanisms may be acting on these two colour classes in darters.

Iranocichla persa, a new cichlid species from southern Iran (Teleostei, Cichlidae).

Iranocichla persa sp. n. is described from the Shur, Hasanlangi and Minab River drainages flowing into the Persian Gulf at the Strait of Hormuz in southern Iran. It is distinguished from Iranocichla hormuzensis, from the Mehran River drainage, by nuptial males having a bright orange breast and lower part of the head (vs. black), a poorly developed or invisible (vs. distinctive) “Tilapia-mark” in the dorsal fin and very clear white spots making almost wavy bars or stripes on the caudal fin (vs. without or with very few white spots). Mitochondrial DNA sequence characters suggest that both Iranocichla species are closely related but form two distinct clades, diagnosable by several fixed mutations in ND2, D-loop and partially by COI sequences. Populations from Kol River drainage, which is situated in-between the Mehran and the Shur River drainages, are more similar to Iranocichla hormuzensis in terms of their male nuptial coloration but to Iranocichla persa sp. n. in their mitochondrial sequence characters. Their status requires further investigation.

Two New and Remarkably Similarly Colored Species ofLabeotropheus(Perciformes: Cichlidae) from Lake Malaŵi, Africa

The haplochromine cichlid genus Labeotropheus is endemic to Lake Malaŵi, Africa. This genus presently contains two recognized species, Labeotropheus fuelleborni and L. trewavasae. As currently recognized, both species consist of geographically isolated populations scattered throughout the lake, each distinguished by a unique male nuptial color pattern. While other such allopatric populations of Lake Malaŵi cichlids have been described as different species, those of Labeotropheus have not, largely due to misunderstandings or misinterpretations of criteria applied to other Malaŵian endemics. Taking a refined approach to the recognition of putative species of Labeotropheus, I used morphometric, meristic, and color characteristics to describe two new, very similarly colored, species of Labeotropheus, both of which are found near Katale Island alongside the Luromo Peninsula in northwestern Lake Malaŵi.

Systematics and Taxonomy of the Snubnose Darter,Etheostoma simoterum(Cope)

Abstract A taxonomic revision of Etheostoma simoterum (Cope) published in 2007 resulted in the recognition of six species, with two species distributed in the Tennessee River system. A newly defined Etheostoma simoterum was restricted to populations in the Holston River above the confluence of the North and South Forks, and the Russell Fork system of the Ohio River drainage. A newly described species, Etheostoma tennesseense Powers & Mayden, included all other populations historically considered Etheostoma simoterum in the Tennessee River system from near the mouth of the Duck River upstream to the Clinch River, including the Holston River below the forks. A subsequent study utilizing molecular phylogenetics and analysis of male nuptial coloration did not support the recognition of Etheostoma tennesseense. Molecular phylogenies resolve both Etheostoma simoterum and Etheostoma tennesseense as paraphyletic. In addition, it was determined that male coloration patterns are not diagnostic for the more restrict...