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Melanin-based plumage coloration and flight displays in plovers and allies.

Plovers and their allies exhibit an impressive diversity of melanin-based plumage patterns ranging from non-melanized to completely melanized species. We use phylogenetic comparative methods to test whether melanization has evolved in relation to sexual selection for attracting mates, to selection for signalling territory defence, or to natural selection for camouflage. First, according to sexual-selection theory, melanized plumage has evolved to amplify the courtship displays of males. As predicted by this hypothesis, we found that males with aerial displays had more melanized plumage than males of ground-displaying species. In addition, sexual dimorphism in melanization was greater in species with display flights than in species with ground displays. Second, melanization may have evolved through social interactions to signal competitive ability in territory defence. We did not find evidence for this hypothesis, since breeding density was unrelated to the melanization of either sex. Finally, melanized plumage may camouflage the incubating parent. The latter hypothesis was not supported, since melanization was unrelated either to the darkness of nest substrate or the extent of vegetation cover. Taken together, our results are most consistent with the sexual-selection hypothesis, and suggest that melanized plumage has evolved to enhance the aerial displays of male plovers.

Animal Communication↗

Evolutionarily labile responses to a signal of aggressive intent.

Males of many swordtail species possess vertical bar pigment patterns that are used both in courtship and agonistic interactions. Expression of the bars may function as a conventional threat signal during conflicts with rival males; bars intensify at the onset of aggression and fade in the subordinate male at contest's end. We used mirror image stimulation and bar manipulations to compare the aggressive responses of the males of four swordtail species to their barred and barless images. We found that having a response to the bars is tightly linked to having genes for bars, while the nature of the response the bars evoked varied across species. Specifically, we report the first known instance where closely related species exhibited differing and contradictory responses to a signal of aggressive motivation. Demonstrating that a signal conveys the same information across species (aggressive intent) while the response to that information has changed among species suggests that the nature of the responses are more evolutionarily labile than the signal.

Aggression↗

Remarkable iridescence in the hindwings of the damselfly Neurobasis chinensis chinensis (Linnaeus) (Zygoptera: Calopterygidae).

The bright green dorsal iridescence of the hindwings of Neurobasis chinensis chinensis males, very rare in Odonata, is known to play a significant role in their courtship behaviour. The mechanism responsible for such high contrast and spectrally pure colour has been investigated and found to be optical interference, producing structural colour from distinct laminations in the wing membrane cuticle. The ventral sides of these iridescent wings are dark brown in colour. In a single continuous membrane of wing cuticle, this is an effect that requires a specialized structure. It is accomplished through the presence of high optical absorption (kappa = 0.13) within two thick layers near the ventral surface of the wing, which leads to superior dorsal colour characteristics. By simultaneously fitting five sets of optical reflectivity and transmissivity spectra to theory, we were able to extract very accurate values of the complex refractive index for all three layer types present in the wing. The real parts of these are n = 1.47, 1.68 and 1.74. Although there is often similarly significant dorsal and ventral colour contrast in other structurally coloured natural systems, very few system designs comprise only a single continuous membrane.

Animals↗

Sexual conflict and anti-aphrodisiac titre in a polyandrous butterfly: male ejaculate tailoring and absence of female control.

Males of the green-veined butterfly Pieris napi synthesize and transfer the volatile methyl salicylate (MeS) to females at mating, a substance that is emitted by non-virgin females when courted by males, curtailing courtship and decreasing the likelihood of female re-mating. The volatile is released when females display the 'mate-refusal' posture with spread wings and elevated abdomen, when courted by conspecific males. Here, we assess how the amount of MeS released by courted females changes over time since mating, and whether it is influenced by the frequency with which females display the mate-refusal posture. We also assess whether males tailor the anti-aphrodisiac content of ejaculates with respect to the expected degree of sperm competition, by comparing how males allocate MeS proportionately to first and second ejaculates in relation to ejaculate mass. The results show that females housed for 5 days in individual cages where they were able to fly and oviposit normally, released similar amounts of MeS. However, females housed together for the same period of time, causing them to frequently display the mate-refusal posture, released significantly lower levels of MeS than the individually housed females. This indicates that female display of the mate-refusal posture depletes their anti-aphrodisiac stores, and suggests that females are unable to voluntarily control their release of the anti-aphrodisiac. A comparison of relative proportion of MeS transferred by males in their first and second ejaculates showed that proportionately more MeS was allocated to the first ejaculate, in accordance with the idea that these are tailored to delay female re-mating.

Analysis of Variance↗

Decreased sexual signalling reveals reduced viability in small populations of the drumming wolf spider Hygrolycosa rubrofasciata.

One of the important goals in conservation biology is to determine reliable indicators of population viability. Sexual traits have been suggested to indicate population extinction risk, because they may be related to viability through condition dependence. Moreover, condition-dependent sexual traits may be more sensitive indicators of population viability than early life-history traits, because deleterious fitness effects of inbreeding tend to be expressed mainly at the end of the species' life history. However, empirical evidence of the significance of sexual behaviour for population viability is missing. In this study, we examined two male sexual traits and survival in 39 different-sized and isolated natural populations of the wolf spider, Hygrolycosa rubrofasciata. We also used several traits to estimate female reproductive success in 25 populations of H. rubrofasciata. According to previous studies, H. rubrofasciata males have a costly and condition-dependent acoustic signal, courtship drumming, which is the target of female choice. Males with a high drumming rate have considerably higher viability than males with a low drumming rate, and females that mate with the more actively drumming males gain genetic benefits in terms of increased offspring viability. Our results show that males in small populations had both lower survival and lower drumming rate than males in larger populations. However, we did not find any evidence for a decline in important early life-history traits (offspring number, hatching success or offspring body mass) or female body mass in small populations. Our results have two important messages for conservation biology. First, they show that sexual traits can be used as sensitive indicators of population viability. Second, the indirect benefits of female choice in terms of good genes might partially compensate for the reduction of viability in declining populations. Also, our results support the view that deleterious effects of small population size are expressed at the end of the species' life history.

Animal Communication↗

Female starlings adjust primary sex ratio in response to aromatic plants in the nest.

Adjustment of offspring sex ratios should be favoured by natural selection when parents are capable of facultatively altering brood sex ratios and of recognizing the circumstances that predict the probable fitness benefit of producing sons and daughters. Although experimental studies have shown that female birds may adjust offspring sex ratios in response to changes in their own condition and in the external appearance of their mate, and male attributes other than his external morphology are also thought to act as signals of male quality, it is not known whether females will respond to changes in such signals, in the absence of any change in the appearance of the male himself. Here, we experimentally manipulated a male courtship display, the green plants carried to the nest by male spotless starlings (Sturnus unicolor), without changing any physical attributes of the male himself, and examined whether this influenced female decisions on offspring sex ratio. We found that in an environment in which female starlings were producing more daughters than sons, experimental enhancement of the green nesting material caused females to significantly increase the number of male eggs produced and thereby removed the female bias. This effect was consistent in 2 years and at two localities. This demonstrates that the green material, whose function has long puzzled biologists, conveys important information to the female and that she facultatively adjusts offspring production accordingly.

Animals↗

Selection on insect immunity in the wild.

The strength of selection on immune function in wild populations has only been examined in a few vertebrate species. We report the results from a study measuring selection on a key insect immune enzyme, phenoloxidase (PO), in a wild population of the damselfly Calopteryx xanthostoma. We followed individually marked males from the pre-reproductive adult phase and recorded their lifetime mating success. We found positive selection on PO activity in response to an immune insult, but no selection on wing-spot quality, a trait actively displayed to females during courtship. We suggest that positive selection on PO activity in the year of study may be explained by annual fluctuations in parasite loads.

Animals↗

Playback of colony sound alters the breeding schedule and clutch size in zebra finch (Taeniopygia guttata) colonies.

The hypothesis that social stimulation, derived from the presence and activities of conspecifics, can hasten and synchronize breeding in colonies of birds was tested. A modified playback/recorder system was used to continuously exaggerate the amount of colony sound available to zebra finches throughout their courtship period. Males that heard 'sound supplements' generated from their own colony sang more than males in control colonies that did not receive playback; males that heard samples from a different colony, sang at an intermediate level. Females that were exposed to the vocalizations of their mate and playback from a colony other than their own, laid eggs earlier and more synchronously than females in control colonies. Females that heard the vocalizations of their mate along with playback samples generated from their own colony, laid eggs more synchronously but not earlier than control females. Both acoustic treatments caused females to lay larger clutches. Social stimulation influences the breeding schedule and clutch size in zebra finch colonies. If there are advantages associated with these effects, social stimulation may contribute to the maintenance of colonial breeding systems.

Acoustic Stimulation↗

Assessing putative interlocus sexual conflict in Drosophila melanogaster using experimental evolution.

The theoretical foundation of sexually antagonistic coevolution is that females suffer a net fitness cost through their interactions with males. The empirical prediction is that direct costs to female lifetime fecundity will exceed indirect benefits despite a possible increase in the genetic quality of offspring. Although direct costs of males have been repeatedly shown, to date no study has comprehensively tested whether females are compensated for this direct harm through indirect benefits. Here we use experimental evolution to show that a mutation giving Drosophila melanogaster females nearly complete resistance to the direct costs of male courtship and remating, but which also excluded almost all indirect benefits, is strongly favoured by selection. We estimated the selection coefficient favouring the resistance allele to be +20%. These results demonstrate that any indirect benefits that females accrued were not sufficient to counter-balance the direct costs of males, and reinforce a large body of past studies by verifying interlocus sexual conflict in this model system.

Analysis of Variance↗

Phenotypic differentiation and pre-mating isolation between allopatric populations of Girardinichthys multiradiatus.

Sexual selection may lead to reproductive isolation between populations through divergence in female mate choice, and population differentiation driven by female mate choice is expected to produce pre- but not post-mating isolation. We tested these hypotheses by looking at whether allopatric populations of the Amarillo (Girardinichthys multiradiatus), a sexually dimorphic viviparous fish with effective female choice, (i) have undergone phenotypical differentiation that may be attributed to divergence in female mate choice, and (ii) are already separated by pre- and/or post-mating reproductive barriers. We found substantial divergence in morphological traits which are the target of female mate choice, and in male courtship behaviour. Strong female preferences for homogametic males indicate substantial and symmetric pre-copulatory isolation, but the few successful heterogametic crosses produced in confinement yielded litters of the same size as those produced in homogametic matings, suggesting that post-copulatory isolation between populations is non-existent or weak. It appears that the studied populations have undergone incipient speciation with a pattern that is consistent with speciation driven by sexual selection, yet further work should assess whether divergence in female preferences has promoted male phenotypic differentiation or whether variation in male attributes has driven divergence in female preferences.

Animals↗

Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster.

Theory predicts that males will benefit when they bias their mating effort towards females of higher reproductive potential, and that this discrimination will increase as males become more resource limited. We conducted a series of experiments to test these predictions in a laboratory population of the fruitfly, Drosophila melanogaster. In this species, courtship and copulation have significant costs to males, and females vary greatly in fecundity, which is positively associated with body size. When given a simultaneous choice between small and large virgin females, males preferentially mated with larger, more fecund, females. Moreover, after males had recently mated they showed a stronger preference for larger females. These results suggest that male D. melanogaster adaptively allocate their mating effort in response to variation in female quality and provide some of the first support for the theoretical prediction that male stringency in mate choice increases as resources become more limiting.

Adaptation, Physiological↗

Detection of infrasound and linear acceleration in fishes.

Fishes have an acute sensitivity to extremely low-frequency linear acceleration, or infrasound, even down to below 1 Hz. The otolith organs are the sensory system responsible for this ability. The hydrodynamic noise generated by swimming fishes is mainly in the infrasound range, and may be important in courtship and prey predator interactions. Intense infrasound has a deterring effect on some species, and has a potential in acoustic barriers. We hypothesize that the pattern of ambient infrasound in the oceans may be used for orientation in migratory fishes, and that pelagic fishes may detect changes in the surface wave pattern associated with altered water depth and distant land formations. We suggest that the acute sensitivity to linear acceleration could be used for inertial guidance, and to detect the relative velocity of layered ocean currents. Sensitivity to infrasound may be a widespread ability among aquatic organisms, and has also been reported in cephalopods and crustaceans.

Animals↗

Evolutionary transitions in parental care and live bearing in vertebrates.

We provide the first review of phylogenetic transitions in parental care and live bearing for a wide variety of vertebrates. This includes new analyses of both numbers of transitions and transition probabilities. These reveal numerous transitions by shorebirds and anurans toward uniparental care by either sex. Whereas most or all of the shorebird transitions were from biparental care, nearly all of the anuran transitions have been from no care, reflecting the prevalence of each form of care in basal lineages in each group. Teleost (bony) fishes are similar to anurans in displaying numerous transitions toward uniparental contributions by each sex. Whereas cichlid fishes have often evolved from biparental care to female care, other teleosts have usually switched from no care to male care. Taxa that have evolved exclusive male care without courtship-role reversal are characterized by male territoriality and low costs of care per brood. Males may therefore benefit from care through female preference of parental ability in these species. Primates show a high frequency of transitions from female care to biparental care, reflecting the prevalence of female care in basal lineages. In the numerous taxa that display live bearing by females, including teleosts, elasmobranchs, squamate reptiles and invertebrates, we find that live bearing has always evolved from a lack of care. Although the transition counts and probabilities will undoubtedly be refined as phylogenetic information and methodologies improve, the overall biases in these taxa should help to place adaptive hypotheses for the evolution of care into a stronger setting for understanding directions of change.

Amphibians↗

Behavioural and ecological consequences of limited attention.

Ecological research in the past few decades has shown that most animals acquire and respond adaptively to information that affects survival and reproduction. At the same time, neurobiological studies have established that the rate of information processing by the brain is much lower than the rate at which information is encountered in the environment, and that attentional mechanisms enable the brain to focus only on the most essential information at any given time. Recent integration of the ecological and neurobiological approaches helps us to understand key behaviours with broad ecological and evolutionary implications. Specifically, current data indicate that limited attention affects diet choice and constrains animals' ability simultaneously to feed and attend to predators. Recent experiments also suggest that limited attention influences social interactions, courtship and mating behaviour.

Animals↗

Assessing sexual conflict in the Drosophila melanogaster laboratory model system.

We describe a graphical model of interlocus coevolution used to distinguish between the interlocus sexual conflict that leads to sexually antagonistic coevolution, and the intrinsic conflict over mating rate that is an integral part of traditional models of sexual selection. We next distinguish the 'laboratory island' approach from the study of both inbred lines and laboratory populations that are newly derived from nature, discuss why we consider it to be one of the most fitting forms of laboratory analysis to study interlocus sexual conflict, and then describe four experiments using this approach with Drosophila melanogaster. The first experiment evaluates the efficacy of the laboratory model system to study interlocus sexual conflict by comparing remating rates of females when they are, or are not, provided with a spatial refuge from persistent male courtship. The second experiment tests for a lag-load in males that is due to adaptations that have accumulated in females, which diminish male-induced harm while simultaneously interfering with a male's ability to compete in the context of sexual selection. The third and fourth experiments test for a lag-load in females owing to direct costs from their interactions with males, and for the capacity for indirect benefits to compensate for these direct costs.

Animals↗

Romantic love: a mammalian brain system for mate choice.

Mammals and birds regularly express mate preferences and make mate choices. Data on mate choice among mammals suggest that this behavioural 'attraction system' is associated with dopaminergic reward pathways in the brain. It has been proposed that intense romantic love, a human cross-cultural universal, is a developed form of this attraction system. To begin to determine the neural mechanisms associated with romantic attraction in humans, we used functional magnetic resonance imaging (fMRI) to study 17 people who were intensely 'in love'. Activation specific to the beloved occurred in the brainstem right ventral tegmental area and right postero-dorsal body of the caudate nucleus. These and other results suggest that dopaminergic reward and motivation pathways contribute to aspects of romantic love. We also used fMRI to study 15 men and women who had just been rejected in love. Preliminary analysis showed activity specific to the beloved in related regions of the reward system associated with monetary gambling for uncertain large gains and losses, and in regions of the lateral orbitofrontal cortex associated with theory of mind, obsessive/compulsive behaviours and controlling anger. These data contribute to our view that romantic love is one of the three primary brain systems that evolved in avian and mammalian species to direct reproduction. The sex drive evolved to motivate individuals to seek a range of mating partners; attraction evolved to motivate individuals to prefer and pursue specific partners; and attachment evolved to motivate individuals to remain together long enough to complete species-specific parenting duties. These three behavioural repertoires appear to be based on brain systems that are largely distinct yet interrelated, and they interact in specific ways to orchestrate reproduction, using both hormones and monoamines. Romantic attraction in humans and its antecedent in other mammalian species play a primary role: this neural mechanism motivates individuals to focus their courtship energy on specific others, thereby conserving valuable time and metabolic energy, and facilitating mate choice.

Animals↗

Evidence of parental care as a newly identified reproductive isolating barrier.

Variation in behavior can contribute to reproductive isolation by preventing gene flow among populations. Here, we tested the novel hypothesis that parental care, when dysregulated, can function as a reproductive isolating mechanism in three-spined stickleback fish (Gasterosteus aculeatus). In the typical "common" stickleback ecotype, males provide care to their offspring by fanning with their pectoral fins and defending their nest. In contrast, a divergent "white" stickleback ecotype has evolutionarily lost care and disperses embryos into the surrounding environment. We examined how paternal care from common, white, and F1 hybrid fathers influenced offspring survival. We detected no intrinsic incompatibilities in embryos, but F1 hybrid fathers exhibited dysregulated parental care that coincided with decreased survival of parented offspring. The increased offspring mortality may be explained by further dysregulation of feeding and parenting circuitry, as F2 hybrids exhibited significantly higher rates of post-fertilization filial cannibalism than common or white fathers. Additionally, despite strong divergence in nesting-building and courtship behavior, F1 hybrids achieved mating success at a similar rate as male commons and whites, suggesting that prezygotic barriers against hybrids may be weak. The observed postzygotic isolation, and potentially weak prezygotic isolation in lab-based studies, suggest that hybridization is likely occurring at low rates in the wild. Population genetic analysis supported this, as low proportions of putative hybrids were detected in sympatric sites. Together, these results may help explain why genetic divergence between these phenotypically distinct ecotypes is low and provide evidence that dysregulated parental behavior can act as a newly discovered postzygotic reproductive isolating barrier.

Reproductive isolation↗

Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor.

The accessory gland of male insects is a genital tissue that secretes many components of the ejaculatory fluid, some of which affect the female's receptivity to courtship and her rate of oviposition. We have examined the structure and expression of two tightly linked genes that are expressed exclusively in the male accessory glands of adult Drosophila melanogaster. The two genes are transcribed from the same strand of DNA, and are separated by 20 bases. Both genes are regulated by the sex determination hierarchy and are expressed in the absence of germ cells. Immunological analysis reveals the protein products of at least one of these genes in the secretion of the accessory gland. The proteins are transferred to the female fly during copulation and are rapidly altered in the female genital tract. The predicted sequence of one protein has features of a peptide hormone precursor, and a region in which 11 of 17 amino acids are identical to egg-laying hormone (ELH) of the California sea hare, Aplysia californica.

Amino Acid Sequence↗