Male Breeding Coloration Research Articles

Sperm of more colourful males are better adapted to ovarian fluids in lake char (Salmonidae).

Fish often spawn eggs with ovarian fluids that have been hypothesized to support the sperm of some males over others (cryptic female choice). Alternatively, sperm reactions to ovarian fluids could reveal male strategies. We used wild-caught lake char (Salvelinus umbla) to experimentally test whether sperm react differently to the presence of ovarian fluid, and whether any differential sperm reaction could be predicted by male breeding coloration, male inbreeding coefficients (based of 4150 SNPs) or the kinship coefficients between males and females. Male coloration was positively linked to body size and current health (based on lymphocytosis and thrombocytosis) but was a poor predictor of inbreeding or kinship coefficients. We found that sperm of more colourful males were faster in diluted ovarian fluids than in water only, while sperm of paler males were faster in water than in ovarian fluids. We then let equal numbers of sperm compete for fertilizations in the presence or absence of ovarian fluids and genetically assigned 1464 embryos (from 70 experimental trials) to their fathers. The presence of ovarian fluids significantly increased the success of the more colourful competitors. Sperm of less inbred competitors were more successful when tested in water only than in diluted ovarian fluids. The kinship coefficients had no significant effects on sperm traits or fertilization success in the presence of ovarian fluids, although parallel stress tests on embryos had revealed that females would profit more from mating with least related males rather than most coloured ones. We conclude that sperm of more colourful males are best adapted to ovarian fluids, and that the observed reaction norms suggest male strategies rather than cryptic female choice.

All in all its just another branch in the tree: A new species of Acanthocercus Fitzinger, 1843 (Squamata: Agamidae), from Angola.

Recent integrative taxonomic studies of the agamid genus Acanthocercus Fitzinger, 1843 have shown that Angola harbors three different taxa, all within the Acanthocercus atricollis (Smith, 1849) species complexA. cyanocephalus (Falk, 1925) in the northeastern parts of the country, A. margaritae Wagner et al. 2021 in the southern regions, and an unnamed species in the central and northwestern parts of Angola. Using the previously published molecular data as evidence of phylogenetic support and newly collected morphological, meristic and coloration data, we here describe this unnamed lineage as a new species. The new species is morphologically very similar to A. cyanocephalus, but it can easily be differentiated from the latter by the coloration pattern of displaying males, with a blue coloration restricted to the head region, and by its inferior scale counts compared to other species of the A. atricollis complex group. As reported in other studies in this group, male breeding coloration is an effective trait for diagnosing these morphologically conserved species. This description raises the number of Acanthocercus species recognized to 15 and is another contribution revealing the rich but still incompletely described herpetological diversity of Angola.

Neural innervation as a potential trigger of morphological color change and sexual dimorphism in cichlid fish

Many species change their coloration during ontogeny or even as adults. Color change hereby often serves as sexual or status signal. The cellular and subcellular changes that drive color change and how they are orchestrated have been barely understood, but a deeper knowledge of the underlying processes is important to our understanding of how such plastic changes develop and evolve. Here we studied the color change of the Malawi golden cichlid (Melanchromis auratus). Females and subordinate males of this species are yellow and white with two prominent black stripes (yellow morph; female and non-breeding male coloration), while dominant males change their color and completely invert this pattern with the yellow and white regions becoming black, and the black stripes becoming white to iridescent blue (dark morph; male breeding coloration). A comparison of the two morphs reveals that substantial changes across multiple levels of biological organization underlie this polyphenism. These include changes in pigment cell (chromatophore) number, intracellular dispersal of pigments, and tilting of reflective platelets (iridosomes) within iridophores. At the transcriptional level, we find differences in pigmentation gene expression between these two color morphs but, surprisingly, 80% of the genes overexpressed in the dark morph relate to neuronal processes including synapse formation. Nerve fiber staining confirms that scales of the dark morph are indeed innervated by 1.3 to 2 times more axonal fibers. Our results might suggest an instructive role of nervous innervation orchestrating the complex cellular and ultrastructural changes that drive the morphological color change of this cichlid species.

The genetics of mate preferences in hybrids between two young and sympatric Lake Victoria cichlid species.

The genetic architecture of mate preferences is likely to affect significant evolutionary processes, including speciation and hybridization. Here, we investigate laboratory hybrids between a pair of sympatric Lake Victoria cichlid fish species that appear to have recently evolved from a hybrid population between similar predecessor species. The species demonstrate strong assortative mating in the laboratory, associated with divergent male breeding coloration (red dorsum versus blue). We show in a common garden experiment, using DNA-based paternity testing, that the strong female mate preferences among males of the two species are fully recovered in a large fraction of their F2 hybrid generation. Individual hybrid females often demonstrated consistent preferences in multiple mate choice trials (more than or equal to five) across a year or more. This result suggests that female mate preference is influenced by relatively few major genes or genomic regions. These preferences were not changed by experience of a successful spawning event with a male of the non-preferred species in a no-choice single-male trial. We found no evidence for imprinting in the F2 hybrids, although the F1 hybrid females may have been imprinted on their mothers. We discuss this nearly Mendelian inheritance of consistent innate mate preferences in the context of speciation theory.

Intrasexual competition underlies sexual selection on male breeding coloration in the orangethroat darter, Etheostoma spectabile.

Elaborate, sexually dimorphic traits are widely thought to evolve under sexual selection through female preference, male–male competition, or both. The orangethroat darter (Etheostoma spectabile) is a sexually dichromatic fish in which females exhibit no preferences for male size or coloration. We tested whether these traits affect individual reproductive success in E. spectabile when multiple males are allowed to freely compete for a female. The quality and quantity of male coloration were associated with greater success in maintaining access to the female and in spawning as the primary male (first male to participate). On the other hand, sneaking behavior showed little correlation with coloration. Male breeding coloration in E. spectabile may therefore demonstrate how intrasexual competition can be a predominant factor underlying the evolution of male ornaments.

Life History Traits of the Mirror Shiner,Notropis spectrunculus, in Western North Carolina

Abstract We investigated the life history of Notropis spectrunculus (Mirror Shiner) at 4 locations in the Tennessee River drainage in western North Carolina that we sampled monthly over 7 months. Specimens were collected by seining and examined to identify age, growth, reproductive patterns, and feeding habits. Sexual maturity occurred at approximately 1 year of age. Spawning occurred from April to July with 13–331 mature oocytes (mean = 115.53, SD = 75.36), and male breeding coloration was present in specimens collected in May, June, and July. Gut contents consisted mainly of insect fragments, primarily Coleoptera and Diptera. Fish were found to inhabit water 0.5–0.75 m deep with sandy substrate, directly below flow-disrupting objects.

Pygmy chameleons of the Rhampholeon platyceps compex (Squamata: Chamaeleonidae): description of four new species from isolated 'sky islands' of northern Mozambique.

The taxonomic status of recently discovered populations of pygmy chameleons (Rhampholeon) from the northern Mozambique montane isolates of Mt. Chiperone, Mt. Mabu, Mt. Inago and Mt. Namuli are assessed, and compared with the closest geographical congeners, including Rhampholeon platyceps Günther 1893 from Mt. Mulanje, and Rh. chapmanorum Tilbury 1992 from the Malawi Hills, both in southern Malawi. Relationships were examined using morphological features and a phylogenetic analysis incorporating two mitochondrial and one nuclear marker. The phylogeny showed that each montane isolate contained a distinct, well-supported clade of chameleons. Chameleons from the Mozambican montane isolates are within a monophyletic clade inclusive of species from southern Malawi (Rh. platyceps and Rh. chapmanorum). Although some relationships are unresolved, the southern Malawi and Mozambican isolates appear to share their most recent common ancestor with species from the Eastern Arc Mountains and Southern Highlands of Tanzania and Malawi (Rh. moyeri, Rh. uluguruesis, Rh. nchisiensis). Along with Rh. beraduccii and Rh. acuminatus, all are included in the subgenus Rhinodigitum. Sister to this larger clade are species from west/central Africa (Rh. temporalis, Rh. spectrum) and the Rh. marshalli-gorongosae complex from southwest Mozambique and adjacent Zimbabwe. Morphological and molecular results confirm that Brookesia platyceps carri Loveridge 1953 is a junior subjective synonym of Rhampholeon platyceps Günther 1892. Historical records of Rh. platyceps from the Shire Highlands (Chiromo) and the Zomba Plateau, are incorrect and the species is now considered endemic to the Mulanje massif. All of the four newly discovered, isolated populations are genetically and morphologically distinct, and we take the opportunity to describe each as a new species. Rhampholeon (Rhinodigitum) maspictus sp. nov. is restricted to Mt. Mabu and distinguished by its large size, well-developed dorsal crenulations, and bright male breeding coloration; Rhampholeon (Rhinodigitum) nebulauctor sp. nov. is restricted to Mt. Chiperone and distinguished by its small size, weakly-developed dorsal crenulations, and a large rostral process in males; Rhampholeon (Rhinodigitum) tilburyi sp. nov. is restricted to Mt. Namuli and distinguished by its small size, weakly-developed dorsal crenulations, and prominent flexure of the snout in males; and Rhampholeon (Rhinodigitum) bruessoworum sp. nov. is restricted to Mt. Inago and distinguished by its small size, weakly-developed dorsal crenulations, large rostral process in males, and relatively long tail in both sexes.

Patterns of Male Breeding Color Variation Differ across Species, Populations, and Body Size in Rainbow and Orangethroat Darters

Sexually dimorphic coloration has been widely suggested to play a role in sexual selection and speciation. Animal colors can originate from several different biochemical pathways, which may underlie different patterns of selection and diversification. Darters of the speciose genus Etheostoma exhibit substantial diversity in male breeding coloration. We used digital photography and image software to comprehensively quantify male coloration in the Rainbow Darter (Etheostoma caeruleum) and the Orangethroat Darter (E. spectabile). Color traits differed across species, populations, and body sizes, with size differences contributing the most to individual color variation. The bluish colors were overall more strongly correlated with size than the reddish colors. Conversely, the reddish colors tended to be less correlated with size and better indicators of species and population identity. Finally, we determined that the bluish colored tissue contained a chromoprotein pigment, and that the reddish colored tissue c...

Attractive males have faster sperm in three-spined sticklebacks Gasterosteus aculeatus

Abstract Recent studies have revealed that sexually selected traits may signal sperm quality and hence male fertilisation ability. There is also evidence that the expression of male sexual ornamentation and associated sperm characteristics depend on an individual’s ability to cope with oxidative stress. Carotenoids are known for their antioxidant properties and carotenoid-based ornaments might represent honest signals as these pigments can be traded off between the investment in sexual ornamentation, sperm function as well as immune response. In this study, we examined the relationship between sexual ornamentation (breeding coloration) and sperm characteristics (e.g., velocity and morphology) in the three-spined stickleback Gasterosteus aculeatus, an externally fertilising fish species, in which sperm competition commonly occurs. During the breeding season males are sperm limited and develop a conspicuous carotenoid-based coloration, which is under strong pre-copulatory sexual selection due to female mate choice and male-male competition. The results of the present study show that the expression of stickleback male breeding coloration is significantly positively associated with the linearity of sperm movement, whereas sperm morphology (head length to tail length ratio) is significantly negatively related to the trajectory of sperm movement. Moreover, there is some support for the phenotype-linked fertility hypothesis as the intensity of male red breeding coloration is significantly positively correlated with sperm velocity, which is supposed to be an important determinant of fertilisation success in external fertilisers, indicating the honesty of the sexually selected nuptial red coloration.

The influence of ambient ultraviolet light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus)

Exposure to enhanced levels of ambient ultraviolet (UV) radiation (UVR) can have adverse effects on aquatic organisms including damage at the cellular and molecular level and impairment of development, fecundity and survival. Much research has been conducted on the role of the harmful UVB radiation. However, due to its greater penetration in water the more abundant UVA radiation can also act as an environmental stressor. Little is known about UVR effects on sperm characteristics although sperm cells should be especially prone to UV-induced oxidative stress. Moreover, UV-related changes in oxidative status may affect the phenotypic expression of energetically costly sexual ornaments. We investigated the effects of long-term exposure to ecologically relevant levels of simulated UVA radiation on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Males were assigned to three spectral exposure treatments differing in the UV spectral part so that they received either enhanced, moderate or no UVA radiation. The results reveal that exposure to enhanced ambient UVA levels had detrimental effects on both male breeding coloration and sperm velocity providing evidence that UVR affects traits targeted by pre- and post-copulatory sexual selection. By highlighting the role of UVA as a factor influencing fitness-relevant traits, our findings may contribute to a better understanding of the consequences of current and future levels of solar UVR for mating systems and life history.

A SIGNIFICANT COMPONENT OF AGEING (DNA DAMAGE) IS REFLECTED IN FADING BREEDING COLORS: AN EXPERIMENTAL TEST USING INNATE ANTIOXIDANT MIMETICS IN PAINTED DRAGON LIZARDS

A decade ahead of their time, von Schantz et al. united sexual selection and free radical biology by identifying causal links between deep-rooted physiological processes that dictate resistance to toxic waste from oxidative metabolism (reactive oxygen species, ROS), and phenotypic traits, such as ornaments. Ten years later, these ideas have still only been tested with indirect estimates of free radical levels (oxidative stress) subsequent to the action of innate and dietary antioxidants. Here, we measure net superoxide (a selection pressure for antioxidant production) and experimentally manipulate superoxide antioxidation using a synthetic mimetic of superoxide dismutase (SOD), Eukarion 134 (EUK). We then measure the toxic effect of superoxide in terms of DNA erosion and concomitant loss of male breeding coloration in the lizard, Ctenophorus pictus. Control males suffered more DNA damage than EUK males. Spectroradiometry showed that male coloration is lost in relation to superoxide and covaries with DNA erosion; in control males, these variables explained loss of color, whereas in EUK males, the fading of coloration was unaffected by superoxide and unrelated to DNA damage. Thus, EUK's powerful antioxidation removes the erosion effect of superoxide on coloration and experimentally verifies the prediction that colors reflect innate capacity for antioxidation.

Socially induced tactic change in 2 types of sand goby sneaker males

Male alternative reproductive tactics, like satellite or sneaking tactics, typically parasitize reproductively on a larger resourceholding tactic. In the sand goby, Pomatoschistus minutus, 2 types of sneaker males are known. Sneaker males with melanization, a typical male breeding coloration, have small testes and large sperm-duct glands, and sneaker males without melanization have large testes and small sperm-duct glands. We tested their potential to change into the nest-holding tactic experimentally by keeping them with or without a large nest-holding male. With nest-holding males, neither sneaker male type built nests. However, without nest-holding males, a large proportion of both types of sneaker males built nests and became nest-holders, and all the nest-building nonmelanized sneaker males developed melanization. Furthermore, nest-building nonmelanized sneaker males had larger sperm-duct glands (used to produce a sperm-containing mucus) than nonnest-building nonmelanized sneaker males. However, contrary to our expectation, treatment did not affect testes size. Compared with melanized sneaker males nonmelanized sneaker males tended to have a lower proportion of nest-building males and showed significantly less reproductive activity, especially in the early experimental period. Finally, in a separate experiment, we confirmed that nonmelanized sneaker males that build nests can spawn and tend eggs normally. Taken together, our results suggest that these tactics are not genetically or ontogenetically fixed but condition dependent. However, this does not exclude an underlying genetic variation in phenotype expression. Key words: alternative reproductive strategies, bourgeois, genetic polymorphism, Gobiidae, seminal vesicles, sperm competition. [Behav Ecol]

No evidence for an indirect benefit from female mate preference in Arctic charr Salvelinus alpinus, but female ornamentation decreases offspring viability

Female mate choice is considered an important evolutionary agent, but there has been an ongoing debate over the fitness consequences it produces, especially in species that have a resource-free mating system. We examined a potential fitness benefit resulting from the pre-spawning mate preference in Arctic charr Salvelinus alpinus, a salmonid fish with no parental care. The females were first allowed to discriminate behaviourally between two males presented to them in a free choice test. We then tested with controlled fertilizations whether the females would accrue indirect genetic benefits for their offspring, as measured by embryonic viability, if they had mated with the male they preferred. Both parental identities influenced offspring survivorship, but the females did not consistently prefer the male which gave her the higher reproductive success. Neither was the degree of male red breeding coloration associated with female preference or the observable genetic quality. In contrast, there was a negative relationship between female coloration and her offspring survivorship, suggesting a significant trade-off in resource investment between sexual ornamentation and reproduction. To conclude, the potential indirect fitness consequences arising from females' pre-spawning mate preference seem to be negligible in early stages of development of Arctic charr.

Processes driving male breeding colour and ecomorphological diversification in rainbow skinks: a phylogenetic comparative test

We used a phylogenetic comparative approach to investigate the importance of ecological shifts in the diversification of both signalling traits and ecomorphological traits in a diverse group of Australian skinks (Carlia). First, we tested whether divergence in male breeding coloration is associated with shifts in habitat openness. Second, we examined whether the type or location of male breeding coloration changes predictably with habitat openness. Third, we tested the ecomorphological predictions that body size should vary in relation to habitat openness and that limb length, toe length and head depth should vary with substrate use. Divergence in male breeding coloration was positively associated with shifts in habitat openness. Our results also indicate that species occupying more open habitats tend to use male sexual signals located on lateral body regions and not necessarily on body regions that are potentially more concealed from aerial predators (e.g. chest and throat). With regard to ecomorphological traits, habitat openness appears to have no predictable influence on body size at the inter-specific level, contrary to expectations based on intra-specific studies. However, consistent with functional predictions, we found that preference for rocky habitats is associated with relatively longer hind limb length, presumably due to selection for greater speed and jumping ability on these substrates. Overall, results of this study support the hypothesis that ecological shifts play a central role in promoting morphological diversification.

Demonstrating the Theory of Ecological Speciation in Cichlids

Demonstrating the Theory of Ecological Speciation in Cichlids

Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids.

Divergent natural selection acting on ecological traits, which also affect mate choice, is a key element of ecological speciation theory, but has not previously been demonstrated at the molecular gene level to our knowledge. Here we demonstrate parallel evolution in two cichlid genera under strong divergent selection in a gene that affects both. Strong divergent natural selection fixed opsin proteins with different predicted light absorbance properties at opposite ends of an environmental gradient. By expressing them and measuring absorbance, we show that the reciprocal fixation adapts populations to divergent light environments. The divergent evolution of the visual system coincides with divergence in male breeding coloration, consistent with incipient ecological by-product speciation.

Molecular Phylogeny of the Snubnose Darters, Subgenus Ulocentra (Genus Etheostoma, Family Percidae)

Snubnose darters comprise one of the largest subgenera of the percid genus Etheostoma. Many species are described based on differences in male breeding coloration. Few morphological synapomorphies have been proposed for the subgenus and their relatives, making it difficult to delineate monophyletic clades. The phylogenetic relationships of the 20 snubnose darter species of the subgenus Ulocentra and 11 members of its proposed sister subgenus Etheostoma were investigated with partial mitochondrial DNA sequences including 1033 bp encompassing the entire mitochondrial control region, the tRNA-Phe gene, and part of the 12S rRNA gene. Two hypotheses on the relationship and monophyly of the two subgenera were evaluated. Both maximum-parsimony and neighbor-joining analyses supported monophyly of the subgenus Ulocentra and resolved some species-level relationships. The banded darter, E. zonale, and its sister taxon, E. lynceum, were not closely related to the snubnose darters and appear to be diverged from the other members of the subgenus Etheostoma, fitting their former distinction as the recognized subgenus Nanostoma. The sister group to Ulocentra appears to be a restricted species assemblage within the subgenus Etheostoma containing E. blennioides, E. rupestre, E. blennius, and the E. thalassinum species group. The placement of the harlequin darter, E. histrio, is problematic, and it may represent a basal member of Ulocentra or of the restricted subgenus Etheostoma. Despite recent estimates of divergence times between nominal Ulocentra taxa, each species exhibits its own unique set of mtDNA haplotypes, providing no direct evidence for current genetic exchange between species. The nominal taxa of snubnose darters thus appear to be evolving independently from each other and therefore constitute valid species under the Phylogenetic Species Concept.

Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks.

Fitness costs of signalling are essential in order for reliable sexual signalling to prevail when the interests of the sexes conflict. This means that signalling can be subjected to a life history trade-off between present and future signalling effort. Here, I show that three-spined stickleback males (Gasterosteus aculeatus), who have a single breeding season during which they breed repeatedly, change their red nuptial coloration over the season depending on their body size at the start of breeding. Large males that completed several breeding cycles increased their red coloration over the season, whereas small males, who completed only a few cycles, did not. The increase in coloration was accompanied by an increase in parental success when males were energy constrained, but not when they had access to an unlimited food supply. Red coloration was thus an honest signal of male parental ability despite changes in signal expression when both signalling and parental care were costly and the investments in them changed simultaneously over the reproductive lifetime. However, the honesty of the signal varied over a lifetime. At the penultimate cycle, bright males cannibalized some of their eggs, probably to increase survival to the last cycle, whereas males cared for their offspring independent of coloration at the ultimate cycle.

Male–male competition facilitates female choice in sticklebacks

In many species, secondary sexual characteristics are used in both male–male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three–spined stickleback Gasterosteus aculeatus , male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male–male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male–male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.

Population structure and colour variation of the cichlid fishes Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi

Extremely fine-scale genetic partitioning has recently been detected among populations of Lake Malawi's rock-dwelling cichlids through the study of microsatellite loci. Understanding the mechanisms of genetic differentiation that operate in this rapidly speciating group requires further investigation of the geographic patterns of gene flow and the congruence between morphological and genetic divergence. In pursuit of this goal, genetic variation at four microsatellite loci and variation in male breeding coloration were examined in several populations of Labeotropheus fuelleborni from southern Lake Malawi. Significant genetic differentiation exists among populations (overall FST = 0.063; p = 0.0002). While migration appears unrestricted within continuous rocky patches, deep waters and sandy bays more than 2 km wide act as strong barriers to gene flow. Dispersal of L. fuelleborni appears to follow a stepping-stone model in which the distribution of habitats often constrains migration to one dimension. It is hypothesized that clinal colour variation in the study area has resulted from the secondary contact of divergent lineages, although reproductive isolation between colour variants is not apparent. Relative to shoreline populations, reduced levels of gene flow among populations inhabiting isolated, deep-water islands provides greater opportunities for drift, adaptation to local conditions, or sexual selection to effect genetic differentiation in this species.