Twelve chromatically opponent ganglion cell types in turtle retina

The turtle retina has been extensively used for the study of chromatic processing mechanisms. Color opponency has been previously investigated with trichromatic paradigms, but behavioral studies show that the turtle has ail ultraviolet (UV) channel and a tetrachromatic visual system. Our laboratory has been working ill the characterization of neuronal responses in the retina of vertebrates using stimuli in the UV-visible range of the electromagnetic spectrum. In the present investigation, we recorded color-opponent responses from turtle amacrine and ganglion cells to UV and visible stimuli and extended our previous results that UV color-opponency is present at the level of the inner nuclear layer. We recorded from 181 neurons, 36 of which were spectrally opponent. Among these, there were 10 amacrine (5%), and 26 ganglion cells (15%). Morphological identification of color-opponent neurons was possible for two ganglion cell classes (G17 and G22) and two amacrine cell classes (A22 and A23b). There was a variety of cell response types and a potential for complex processing of chromatic stimuli, with intensity- and wavelength-dependent response components. Ten types of color opponency were found in ganglion cells and by adding previous results from our laboratory, 12 types of opponent responses have been found. The majority of the ganglion cells were R+UVBG- and RG+UVB-color-opponents but there were other less frequent types of chromatic opponency. This study confirms the participation of a UV channel in the processing of color opponency in the turtle inner retina and shows that the turtle visual system has the retinal mechanisms to allow many possible chromatic combinations.

Male and female interactions during courtship of the Neotropical damselfly Mnesarete pudica (Odonata: Calopterygidae)

The courtship behavior in calopterygid damselflies is well documented; however, the behavior of the large Neotropical genus Mnesarete is still unknown. Thus, here we present the first description of male-female interactions in Mnesarete pudica, a common damselfly in the Neotropical Savanna. The male-female interactions were composed of courtship displays, mounting, and chasing. The courtship behavior lasted 5.23 +/- 1.65 s and is very different from other calopterygids, consisting of hovering flights and the cross display made in front of females rather than on the oviposition site. The arrival and presence of females on a male territory are not sufficient to initiate sexual interactions; the male usually interacts with the female only after a patrolling flight. The females may present three distinct behaviors in response to male approach: (a) warding off signal (31.53%), (b) escape (28.83%), (c) and wing flipping (39.64%), which seems to stimulate male courtship. Females also may sit still, which induces males to react as if females were signaling they are willing to mate. In this paper, we also suggest that male courtship behavior is mediated by female signals.

Sexual Differences in the Behavior of the Harvestman Leiobunum vittatum (Opiliones, Sclerosomatidae) Towards Conspecific Cues

Preliminary observations of the harvestman Leiobunum vittatum found that individuals rub their bodies against the substrate, presenting the possibility of chemical marking. To determine whether or not L. vittatum individuals can detect substrate-borne chemical cues, we compared responses of L. vittatum males and females to substrate-borne male and female cues. We found that individuals of L. vittatum do respond to conspecific cues and that their responses are sex-specific. In response to substrate-borne conspecific cues, male L. vittatum spent more time, engaged in more scraping with their sensory legs I, and engaged in pedipalpal tapping more often in the presence versus absence of conspecific cues (male and female equally). Furthermore, in the presence of conspecific cues, males engaged in two behaviors never observed in females-(a) "fast approach" and (b) "jerking", the latter of which was never observed in the presence of cricket cues. In contrast to males, females did not spend more time on conspecific cues, but did spend more time tapping their pedipalps in the presence of male vs female cues, suggesting an ability to distinguish between them. A final experiment explored the possibility that females could discriminate among males of varying histories of agonistic interactions based upon their chemical cues. We found no support for this hypothesis. Our results demonstrate that L. vitattum do respond to conspecific cues, and introduce the possibility that intraspecific communication may be mediated in part by chemical cues.

Sexual selection in Pomatoschistus – nests, sperm competition, and paternal care

Sexual selection arises through variation in reproductive success. This thesis investigates different aspects important in sexual selection, namely nest building, sperm competition, paternity and paternal care, and their mutual interrelationships. In the studied species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), sperm competition did arise when small males, so called sneakers, sneaked into other males nests and released sperm. They seemed to use female behaviour as their prime cue for a sneaking opportunity. However, also nest-holders, both with and without eggs, were found to fertilize eggs in the nests of other males. Clearly, nest-holding males tried to prevent other males from spreading their sperm in their nests, since they showed aggression towards such males. A nest building experiment indicated that the small nest-openings found in the sneaker male treatment were sexually selected through protection against sneaking or by female choice. Yet, no behavioural or genetical support for the hypothesis that the nest functions as a physical or visual defence, or that sneaker males prefer to sneak upon nests with wide nest-openings, were found in the other studies. Still, individual nest-holding males showed a higher mucus preparation effort inside the nest in the presence of a sneaker male than when alone. In close relatives, such mucus contains sperm, suggesting an importance in sperm competition. However, the mucus may also have pheromone and anti-bacterial functions and may constitute a mating effort, as found in other gobies. Both a behavioural and a mate choice experiment suggested that the males were not less eager to spawn in the presence of a sneaker male. Sneak intrusion did not affect nest defence, fanning or filial cannibalism, nor had paternity an effect on filial cannibalism. This and various life history aspects, together with the fact that the parasitic male only fertilized a fraction of the clutches, would predict females to ignore sneaker males. This was also the case, as the presence of sneaker males was found not to affect female spawning decision. Still, several females spawned in two nests, which coincided with parasitic spawnings, suggesting a cost of disturbance for the females and thus a substantial cost to the nest-holding males in terms of lost mating success. However, females paid attention to other traits in their choice of mate since spawning was associated with sand volume of the nest, but not with nest-opening width. Also, female (but not male) courtship was correlated with partial clutch filial cannibalism, indicating that females are able to anticipate future male cannibalism. In a partial correlation of nest opening, sand volume, male courtship display, displacement fanning and male size, a large number of traits were correlated both positively and negatively with regard to how we may expect them to be appreciated by females. For instance, males which fan well also build large nests or display intensely (but not both). Together with all the other results of this thesis, this shows the entangled selection pressures working on breeding animals, as well as the different male and female tactics employed to maximize their reproduction.

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate-choice experiments, conducted in clear water and under broad-spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference-trait co-evolution in cichlid fish. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 398-406.

Sequential female assessment drives complex sexual selection on bower shape in a cichlid fish

In many animals, sexual selection on male traits results from female mate choice decisions made during a sequence of courtship behaviors. We use a bower-building cichlid fish, Nyassachromis cf. microcephalus, to show how applying standard selection analysis to data on sequential female assessment provides new insights into sexual selection by mate choice. We first show that the cumulative selection differentials confirm previous results suggesting female choice favors males holding large volcano-shaped sand bowers. The sequential assessment analysis reveals these cumulative differentials are the result of selection acting on different bower dimensions during the courtship sequence; females choose to follow males courting from tall bowers, but choose to engage in premating circling with males holding bowers with large diameter platforms. The approach we present extends standard selection analysis by partitioning the variances of increasingly accurate estimates of male reproductive fitness and is applicable to systems in which sequential female assessment drives sexual selection on male traits.

Immune Activation Reduces Sperm Quality in the Great Tit

Mounting an immune response against pathogens incurs costs to organisms by its effects on important life-history traits, such as reproductive investment and survival. As shown recently, immune activation produces large amounts of reactive species and is suggested to induce oxidative stress. Sperm are highly susceptible to oxidative stress, which can negatively impact sperm function and ultimately male fertilizing efficiency. Here we address the question as to whether mounting an immune response affects sperm quality through the damaging effects of oxidative stress. It has been demonstrated recently in birds that carotenoid-based ornaments can be reliable signals of a male's ability to protect sperm from oxidative damage. In a full-factorial design, we immune-challenged great tit males while simultaneously increasing their vitamin E availability, and assessed the effect on sperm quality and oxidative damage. We conducted this experiment in a natural population and tested the males' response to the experimental treatment in relation to their carotenoid-based breast coloration, a condition-dependent trait. Immune activation induced a steeper decline in sperm swimming velocity, thus highlighting the potential costs of an induced immune response on sperm competitive ability and fertilizing efficiency. We found sperm oxidative damage to be negatively correlated with sperm swimming velocity. However, blood resistance to a free-radical attack (a measure of somatic antioxidant capacity) as well as plasma and sperm levels of oxidative damage (lipid peroxidation) remained unaffected, thus suggesting that the observed effect did not arise through oxidative stress. Towards the end of their breeding cycle, swimming velocity of sperm of more intensely colored males was higher, which has important implications for the evolution of mate choice and multiple mating in females because females may accrue both direct and indirect benefits by mating with males having better quality sperm.

Segregation of species-specific male attractiveness in f(2) hybrid lake Malawi cichlid fish

Among the huge radiations of haplochromine cichlid fish in Lakes Malawi and Victoria, closely related species are often reproductively isolated via female mate choice although viable fertile hybrids can be produced when females are confined only with heterospecific males. We generated F(2) hybrid males from a cross between a pair of closely related sympatric cichlid fish from Lake Malawi. Laboratory mate choice experiments using microsatellite paternity analysis demonstrated that F(2) hybrid males differed significantly in their attractiveness to females of the two parental species, indicating heritable variation in traits involved in mate choice that may contribute to reproductive isolation between these species. We found no significant correlation between male mating success and any measurement of male colour pattern. A simple quantitative genetic model of reproductive isolation suggests that there may be as few as two chromosomal regions controlling species-specific attractiveness. We propose that adaptive radiation of Lake Malawi cichlids could be facilitated by the presence of genes with major effects on mate choice and reproductive isolation.

A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments

BACKGROUND: The sensory drive hypothesis predicts that divergent sensory adaptation in different habitats may lead to premating isolation upon secondary contact of populations. Speciation by sensory drive has traditionally been treated as a special case of speciation as a byproduct of adaptation to divergent environments in geographically isolated populations. However, if habitats are heterogeneous, local adaptation in the sensory systems may cause the emergence of reproductively isolated species from a single unstructured population. In polychromatic fishes, visual sensitivity might become adapted to local ambient light regimes and the sensitivity might influence female preferences for male nuptial color. In this paper, we investigate the possibility of speciation by sensory drive as a byproduct of divergent visual adaptation within a single initially unstructured population. We use models based on explicit genetic mechanisms for color vision and nuptial coloration. RESULTS: We show that in simulations in which the adaptive evolution of visual pigments and color perception are explicitly modeled, sensory drive can promote speciation along a short selection gradient within a continuous habitat and population. We assumed that color perception evolves to adapt to the modal light environment that individuals experience and that females prefer to mate with males whose nuptial color they are most sensitive to. In our simulations color perception depends on the absorption spectra of an individual's visual pigments. Speciation occurred most frequently when the steepness of the environmental light gradient was intermediate and dispersal distance of offspring was relatively small. In addition, our results predict that mutations that cause large shifts in the wavelength of peak absorption promote speciation, whereas we did not observe speciation when peak absorption evolved by stepwise mutations with small effect. CONCLUSION: The results suggest that speciation can occur where environmental gradients create divergent selection on sensory modalities that are used in mate choice. Evidence for such gradients exists from several animal groups, and from freshwater and marine fishes in particular. The probability of speciation in a continuous population under such conditions may then critically depend on the genetic architecture of perceptual adaptation and female mate choice.

Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids

Female mating preference based on male nuptial coloration has been suggested to be an important source of diversifying selection in the radiation of Lake Victoria cichlid fish. Initial variation in female preference is a prerequisite for diversifying selection; however, it is rarely studied in natural populations. In clear water areas of Lake Victoria, the sibling species Pundamilia pundamilia with blue males and Pundamilia nyererei with red males coexist, intermediate phenotypes are rare, and most females have species-assortative mating preferences. Here, we study a population of Pundamilia that inhabits turbid water where male coloration is variable from reddish to blue with most males intermediate. We investigated male phenotype distribution and female mating preferences. Male phenotype was unimodally distributed with a mode on intermediate color in 1 year and more blue-shifted in 2 other years. In mate choice experiments with females of the turbid water population and males from a clearer water population, we found females with a significant and consistent preference for P. pundamilia (blue) males, females with such preferences for P. nyererei (red) males, and many females without a preference. Hence, female mating preferences in this population could cause disruptive selection on male coloration that is probably constrained by the low signal transduction of the turbid water environment. We suggest that if environmental signal transduction was improved and the preference/color polymorphism was stabilized by negative frequency-dependent selection, divergent sexual selection might separate the 2 morphs into reproductively isolated species resembling the clear water species P. pundamilia and P. nyererei.

Assortative mating among Lake Malawi cichlid fish populations is not simply predictable from male nuptial colour

Background: Research on the evolution of reproductive isolation in African cichlid fishes has largely focussed on the role of male colours and female mate choice. Here, we tested predictions from the hypothesis that allopatric divergence in male colour is associated with corresponding divergence in preference. Methods: We studied four populations of the Lake Malawi Pseudotropheus zebra complex. We predicted that more distantly-related populations that independently evolved similar colours would interbreed freely while more closely-related populations with different colours mate assortatively. We used microsatellite genotypes or mesh false-floors to assign paternity. Fisher's exact tests as well as Binomial and Wilcoxon tests were used to detect if mating departed from random expectations. Results: Surprisingly, laboratory mate choice experiments revealed significant assortative mating not only between population pairs with differently coloured males, but between population pairs with similarly-coloured males too. This suggested that assortative mating could be based on nonvisual cues, so we further examined the sensory basis of assortative mating between two populations with different male colour. Conducting trials under monochromatic (orange) light, intended to mask the distinctive male dorsal fin hues (blue v orange) of these populations, did not significantly affect the assortative mating by female P. emmiltos observed under control conditions. By contrast, assortative mating broke down when direct contact between female and male was prevented. Conclusion: We suggest that non-visual cues, such as olfactory signals, may play an important role in mate choice and behavioural isolation in these and perhaps other African cichlid fish. Future speciation models aimed at explaining African cichlid radiations may therefore consider incorporating such mating cues in mate choice scenarios.

Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation

The hypothesis of ecological divergence giving rise to premating isolation in the face of gene flow is controversial. However, this may be an important mechanism to explain the rapid multiplication of species during adaptive radiation following the colonization of a new environment when geographical barriers to gene flow are largely absent but underutilized niche space is abundant. Using cichlid fish, we tested the prediction of ecological speciation that the strength of premating isolation among species is predicted by phenotypic rather than genetic distance. We conducted mate choice experiments between three closely related, sympatric species of a recent radiation in Lake Mweru (Zambia/DRC) that differ in habitat use and phenotype, and a distantly related population from Lake Bangweulu that resembles one of the species in Lake Mweru. We found significant assortative mating among all closely related, sympatric species that differed phenotypically, but none between the distantly related allopatric populations of more similar phenotype. Phenotypic distance between species was a good predictor of the strength of premating isolation, suggesting that assortative mating can evolve rapidly in association with ecological divergence during adaptive radiation. Our data also reveals that distantly related allopatric populations that have not diverged phenotypically, may hybridize when coming into secondary contact, e.g. upon river capture because of diversion of drainage systems.

Hotshots, hot spots, and female preference: exploring lek formation models with a bower-building cichlid fish

In many animals, males congregate in leks that females visit for the sole purpose of mating. We observed male and female behavior on 3 different-sized leks of the bower-building cichlid fish Nyassachromis cf. microcephalus to test predictions of 3 prominent lek models: the "hotshot," "hot spot," and "female preference" models. In this system, we were able to refine these predictions by distinguishing between indirect mate choice, by which females restrict their set of potential mates in the absence of individual male assessment, and direct mate choice, by which females assess males and their territories through dyadic behavioral interactions. On no lek were males holding central territories favored by indirect or direct mate choice, contrary to the prediction of the hotshot model that leks form because inferior males establish territories surrounding hotshot males preferred by females. Average female encounter rate of males increased with lek size, a pattern typically interpreted as evidence that leks form through female preference for lekking males, rather than because males congregate in hot spots of high female density. Female propensity to engage in premating behavior once courted did not increase with lek size, suggesting female preference for males on larger leks operated through indirect choice rather than direct choice based on individual assessment. The frequency of male-male competitive interactions increased with lek size, whereas their foraging rate decreased, implying a cost to males maintaining territories on larger leks. Together these data most strongly support the female preference model, where females may benefit through indirect mate choice for males able to meet the competitive cost of occupying larger leks.

Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish

Hybrid speciation is constrained by the homogenizing effects of gene flow from the parental species. In the absence of post-mating isolation due to structural changes in the genome, or temporal or spatial premating isolation, another form of reproductive isolation would be needed for homoploid hybrid speciation to occur. Here, we investigate the potential of behavioural mate choice to generate assortative mating among hybrids and parental species. We made three-first-generation hybrid crosses between different species of African cichlid fish. In three-way mate-choice experiments, we allowed hybrid and nonhybrid females to mate with either hybrid or nonhybrid males. We found that hybrids generally mated nonrandomly and that hybridization can lead to the expression of new combinations of traits and preferences that behaviourally isolate hybrids from both parental species. Specifically, we find that the phenotypic distinctiveness of hybrids predicts the symmetry and extent of their reproductive isolation. Our data suggest that behavioural mate choice among hybrids may facilitate the establishment of isolated hybrid populations, even in proximity to one or both parental species.

A test of genetic association among male nuptial coloration, female mating preference, and male aggression bias within a polymorphic population of cichlid fish

Both inter- and intrasexual selection have been implicated in the origin and maintenance of species-rich taxa with diverse sexual traits. Simultaneous disruptive selection by female mate choice and male-male competition can, in theory, lead to speciation without geographical isolation if both act on the same male trait. Female mate choice can generate discontinuities in gene flow, while male-male competition can generate negative frequency-dependent selection stabilizing the male trait polymorphism. Speciation may be facilitated when mating preference and/or aggression bias are physically linked to the trait they operate on. We tested for genetic associations among female mating preference, male aggression bias and male coloration in the Lake Victoria cichlid Pundamilia. We crossed females from a phenotypically variable population with males from both extreme ends of the phenotype distribution in the same population (blue or red). Male offspring of a red sire were significantly redder than males of a blue sire, indicating that intra-population variation in male coloration is heritable. We tested mating preferences of female offspring and aggression biases of male offspring using binary choice tests. There was no evidence for associations at the family level between female mating preferences and coloration of sires, but dam identity had a significant effect on female mate preference. Sons of the red sire directed significantly more aggression to red than blue males, whereas sons of the blue sire did not show any bias. There was a positive correlation among individuals between male aggression bias and body coloration, possibly due to pleiotropy or physical linkage, which could facilitate the maintenance of color polymorphism.