Mechanisms of sperm competition

Sperm competition occurs when two (or more) males inseminate a single female during a reproductive cycle, but what determines which one of them will fertilize her eggs? Is it simply a lottery, or are there some more complex rules by which matings are translated into offspring? Several studies covering various animal groups have shown that mating order effects are often important in determining paternity patterns: in animals as different as insects and birds, the sperm from the last male to mate often has precedence over previously introduced sperm. Recently, behavioural ecologists and physiologists have started to examine the mechanisms by which sperm precedence is achieved. The study of sperm competition mechanisms complements the more behavioural studies, and a combination of the two approaches used on single species should prove to be particularly rewarding.     

Proximate perspectives on the evolution of female aggression: good for the gander,good for the goose?

Female–female aggression often functions in competition over reproductive or social benefits, but the proximate mechanisms of this apparently adaptive behaviour are not well understood. The sex steroid hormone testosterone (T) and its metabolites are well-established mediators of male–male aggression, and several lines of evidence suggest that T-mediated mechanisms may apply to females as well. However, a key question is whether mechanisms of female aggression primarily reflect correlated evolutionary responses to selection acting on males, or whether direct selection acting on females has made modifications to these mechanisms that are adaptive in light of female life history. Here, I examine the degree to which female aggression is mediated at the level of T production, target tissue sensitivity to T, or downstream genomic responses in order to test the hypothesis that selection favours mechanisms that facilitate female aggression while minimizing the costs of systemically elevated T. I draw heavily from avian systems, including the dark-eyed junco (Junco hyemalis), as well as other organisms in which these mechanisms have been well studied from an evolutionary/ecological perspective in both sexes. Findings reveal that the sexes share many behavioural and hormonal mechanisms, though several patterns also suggest sex-specific adaptation. I argue that greater attention to multiple levels of analysis—from hormone to receptor to gene network, including analyses of individual variation that represents the raw material of evolutionary change—will be a fruitful path for understanding mechanisms of behavioural regulation and intersexual coevolution.     

Sperm competition in mammals

Female promiscuity can lead to the spermatazoa of several males 'competing' to fertilize the ova of a single female. Such promiscuity is relatively common among mammals and has resulted in a suite of adaptations associated with sperm competition. In the last decade, laboratory scientists using experimental techniques have clarified the physiological and behavioural mechanisms that result from sperm competition. Field biologists have collected data on a variety of mammals to test predictions of sperm competition theory. Unfortunately, theories developed and tested in laboratory situations do not always explain variation in behaviour observed in field studies.     

Female control of paternity

Of the two components of sexual selection, female choice is much less obvious than male-male competition, and hence has always been considered to be of secondary importance. However, recent field observations and new theory have brought about a radical change of emphasis. It now appears that although a female's choice of who fathers her offspring often occurs in a subtle manner, it may be widespread and take place through a variety of behavioural and physiological mechanisms, including the manipulation of male behaviour and the selection of sperm within the female reproductive tract.     

Impacts of fever on locust life-history traits: costs or benefits?

Fever, like other mechanisms for defence against pathogens, may have positive and negative consequences for host fitness. In ectotherms, fever can be attained through modified behavioural thermoregulation. Here we examine potential costs of behavioural fever by holding adult, gregarious desert locusts at elevated temperatures simulating a range of fever intensities. We found no effect of fever temperatures on primary fitness correlates of survival and fecundity. However, flight capacity and mate competition were reduced, although there was no relation between time spent at fever temperatures and magnitude of the response. While these effects could indicate a direct cost of fever, they are also consistent with a shift towards the solitaria phase state that, in a field context, could be considered an adaptive life-history response to limit the impact of disease. These conflicting interpretations highlight the importance of considering complex defence mechanisms and trade-offs in an appropriate ecological context.     

Sperm competition and male ejaculate investment in Nauphoeta cinerea: effects of social environment during development

Selective pressure arising from sperm competition has been predicted to influence evolutionary and behavioural adjustment of ejaculate investment, but also may influence developmental adjustment of ejaculate investment. Immature males able to target resources strategically based on the competitive environment they will experience when they become sexually mature should be at a selective advantage. In our study we investigated how the presence of potential competitors or mates affects ejaculate and testes investment during development in the cockroach Nauphoeta cinerea, a species where males control female remating via their ejaculate size (large spermatophores prevent females from remating and therefore function to avoid sperm competition for males) and females store sperm. Our aim was to determine whether the social environment influences developmental adjustment of ejaculate investment and the relative importance of ejaculate components with different functions; avoidance of or engagement in sperm competition. We conclude that the social environment can influence developmental and behavioural flexibility in specific ejaculate components that may function to avoid or engage in sperm competition.     

Heterospecific ovicide influences the outcome of competition between two endoparasitoids, Encarsia formosa and Encarsia luteola

Abstract.  1. Studies of inter-specific competition in parasitoids have largely focused on the outcome of within-host competition and the behavioural mechanisms by which female parasitoids prevent competition. Another, less well studied, possibility is oviposition preceded by 'heterospecific ovicide', the destruction of the other species' egg. Heterospecific ovicide essentially eliminates within-host competition.
2. This study investigated the mechanisms and outcome of within-host competition in Encarsia formosa and Encarsia luteola , solitary endoparasitoids of whitefly pests. These species are known to commit ovicide of conspecific eggs.
3. Competition experiments indicated that the offspring of second-ovipositing females had an apparent advantage in competition, regardless of whether the second female was E. formosa or E. luteola .
4. Observations of ovipositor movement through the cuticle of host whitefly nymphs showed that both species often committed heterospecific ovicide and then oviposited or host-fed. Multiparasitism and heterospecific host discrimination were less common and absent respectively.
5. Heterospecific ovicide appears to explain the second-female advantage in competition between these species. Second-female advantage is contrary to the paradigmatic view of multiparasitism, where the first-ovipositing female has an advantage in competition or one of the species consistently prevails in competition.     

Fetal behaviour and the cardiovascular system

With increasing gestation both in the human and in animals clear fetal behavioural state cycles develop. Fetal heart rate patterns are closely related to the phenomenon of behavioural state. In this review article fetal heart rate patterns will be analysed in relation to particular behavioural states, individual movement patterns and diurnal variations. Attention will also be paid to maturational changes. Differences between human and animal states are emphasized. It is concluded, that understanding of the basic mechanisms underlying the normal heart rate patterns throughout gestation, improves the reliability of fetal surveillance.     

Is separating resource competition from allelopathy realistic?

Allelopathy and resource competition have often been suggested to explain plant-plant interference. Many studies have attempted to separate these two mechanisms of interference to demonstrate either as a probable cause of an observed growth pattern. We, however, are of the opinion that separating allelopathy from resource competition is essentially impossible in natural systems. Furthermore, any experimental design to separate allelopathy and resource competition will create conditions that will never occur in nature. In this article, the ecological interaction between allelopathy and resource competition in natural systems is discussed.     

Frequency dependence and competition

Intraspecific competition implies interaction among the individuals of a population, so natural selection on genotypic variation in characters related to the competition will necessarily be frequency dependent. Intraspecific antagonistic competition exhibits properties similar to other behavioural interactions between individuals. In exploitative intraspecific competition the interactions among individuals are less direct. Exploitation modifies the abundance of the various limiting resources according to the use of these resources by the individual members of the population. The amount of resource available to an individual is therefore a function of the phenotypes present in the population, through their density and frequency.     

A review of relationships between interspecific competition and invasions in fruit flies (Diptera: Tephritidae)

Abstract.  1. A number of invasions in the family Tephritidae (fruit flies) have been observed worldwide despite quarantine procedures. In this review, the potential importance of interspecific competition and competitive displacement among different tephritid species is evaluated in the context of recent invasions.
2. Where polyphagous tephritid species have been introduced in areas already occupied by a polyphagous tephritid, interspecific competition has resulted in a decrease in number and niche shift of the pre-established species. No reciprocal invasions have been observed.
3. The data on tephritid invasions seem to support a hierarchical mode of competition; however, complete exclusion usually did not occur. Indeed, tephritid distribution and abundance are markedly structured by various abiotic (mostly climatic) and biotic (host plants) factors.
4. The primary determinant of competitive interactions in near-optimal conditions, such as lowlands with abundant fruit plantations, is probably the life-history strategy. The r – K gradient could be used as a predictor of potential invaders, because K traits (such as large adult size) may favour both exploitation and interference competition.
5. For future research, a better understanding of competition mechanisms seems essential. Different species competing in the same area should be compared with respect to: (i) demographic parameters, (ii) the outcome of experimental co-infestations on the same fruit, and (iii) behavioural and chemical interference mechanisms.     

The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism

When females are inseminated by more than one male (polyandry) sexual selection continues after insemination in the form of sperm competition and cryptic female choice. The sexually-selected sperm hypothesis proposes that, under the risk of sperm competition, additive variation in male traits determining fertilising efficiency will select for female propensity to be polyandrous in order to increase the probability of producing sons with superior fertilising efficiency. Two factors complicate this prediction: sex-biased transmission of male fertilising efficiency traits and sexual antagonism of sex-limited traits, fostered by sex-biased inheritance. Here, we (i) review the evidence that male traits contributing towards fertilising efficiency are heritable through sex-biased mechanisms, and (ii) explore the evolutionary implications for male and female reproductive strategies caused by both sex-biased transmission and sexual antagonism of fertilising efficiency traits. Many male fertilising efficiency traits are heritable through sex-biased mechanisms and may not necessarily increase female fitness. The predictions of the sexually-selected sperm hypothesis change dramatically under these different mechanisms of inheritance of fertilising efficiency traits, and different fitness pay-offs derived by females from the expression of such traits. Both sex-biased control of fertilising efficiency and sexual antagonism may also be important in explaining the maintenance of the genetic variance and selection potential of fertilising efficiency. We propose that a useful approach to test the sexually-selected sperm hypothesis is to combine studies which identify behavioural and physiological mechanisms explaining variation in reproductive success with artificial selection experiments to infer the underlying evolutionary patterns.     

Converging levels of analysis in the cognitive neuroscience of visual attention.

Experiments using behavioural, lesion, functional imaging and single neuron methods are considered in the context of a neuropsychological model of visual attention. According to this model, inputs compete for representation in multiple visually responsive brain systems, sensory and motor, cortical and subcortical. Competition is biased by advance priming of neurons responsive to current behavioural targets. Across systems competition is integrated such that the same, selected object tends to become dominant throughout. The behavioural studies reviewed concern divided attention within and between modalities. They implicate within-modality competition as one main restriction on concurrent stimulus identification. In contrast to the conventional association of lateral attentional focus with parietal lobe function, the lesion studies show attentional bias to be a widespread consequence of unilateral cortical damage. Although the clinical syndrome of unilateral neglect may indeed be associated with parietal lesions, this probably reflects an assortment of further deficits accompanying a simple attentional imbalance. The functional imaging studies show joint involvement of lateral prefrontal and occipital cortex in lateral attentional focus and competition. The single unit studies suggest how competition in several regions of extrastriate cortex is biased by advance priming of neurons responsive to current behavioural targets. Together, the concepts of competition, priming and integration allow a unified theoretical approach to findings from behavioural to single neuron levels.     

The disruption of dominance hierarchies by a non-native species: an individual-based analysis

We studied the effects of the exotic rainbow trout (Oncorhynchus mykiss) on the performance and the dominance hierarchy of native Atlantic salmon (Salmo salar) at the group and individual level using laboratory and semi-natural experiments. At the group level, we compared the effects of interspecific and intraspecific competition (substitutive and additive design) on behavioural responses and growth of young-of-the-year Atlantic salmon. At the individual level, the same design was used to evaluate: (1) the temporal consistency of behavioural responses, dominance hierarchy and growth rate of Atlantic salmon; (2) the pattern of correlations between behaviours; and (3) the relationship between individual growth rate and behaviour. In the laboratory, group-level analyses revealed a weak but similar effect of rainbow trout and intraspecific competition on the behaviour and growth of Atlantic salmon. In contrast, individual-based analyses demonstrated that rainbow trout (but not intraspecific competition) strongly affected behavioural strategy, dominance hierarchy and growth trajectory of individual Atlantic salmon. Specifically, behaviours, dominance status and growth rate of salmon were temporally consistent in the intraspecific environment, while these patterns were disrupted when rainbow trout were present. Similarly, we found that rainbow trout strongly affected behavioural correlations and the relationships between individual growth rate and behaviour. The semi-natural experiments confirmed these results as interspecific competition affected relationships between individual growth rate of salmon, initial weight and activity index. Overall, individual-based analyses highlighted important mechanisms that were concealed at the group level, and that may be crucial to understand ecological and evolutionary consequences of exotic species. Moreover, these results demonstrated that competition with an exotic species disrupts the hierarchical relationship among native individuals and may therefore represent a potential for a shift in selective pressure.     

Tactic-specific success in sperm competition

Sperm competition is a major force in sexual selection, but its implications for mating-system and life-history evolution are only beginning to be understood. The well-known sneak-guard model predicts that sneaks will win in sperm competition. We now provide empirical confirmation of this prediction. Bluegill sunfish (Lepomis macrochirus) have both sneak (cuckolder) and guard (parental) males. Guards make nests, court females and provide solitary parental care for the embryos. Sneaks include small cuckolders, which are termed 'sneakers', that dart in and out of nests in order to ejaculate between the spawning pair and larger cuckolders, which are termed 'satellites', that mimic females in order to ejaculate between the spawning pair. Using field behavioural data, genetic data and new mathematical models for paternity analyses, we show, for the first time to the authors' knowledge, that sneaks fertilize more eggs than guards during sperm competition. In addition, we show that sneakers are superior to satellites in sperm competition and, thus, that even among sneaks there are tactic-specific differences in competitive success.     

Coexistence of behavioural types in an aquatic top predator: a response to resource limitation?

Intra-population variation in behaviour unrelated to sex, size or age exists in a variety of species. The mechanisms behind behavioural diversification have only been partly understood, but density-dependent resource availability may play a crucial role. To explore the potential coexistence of different behavioural types within a natural fish population, we conducted a radio telemetry study, measuring habitat use and swimming activity patterns of pike (Esox lucius), a sit-and-wait predatory fish. Three behavioural types co-occurred in the study lake. While two types of fish only selected vegetated littoral habitats, the third type opportunistically used all habitats and increased its pelagic occurrence in response to decreasing resource biomasses. There were no differences in size, age or lifetime growth between the three behavioural types. However, habitat-opportunistic pike were substantially more active than the other two behavioural types, which is energetically costly. The identical growth rates exhibited by all behavioural types indicate that these higher activity costs of opportunistic behaviour were compensated for by increased prey consumption in the less favourable pelagic habitat resulting in approximately equal fitness of all pike groups. We conclude that behavioural diversification in habitat use and activity reduces intraspecific competition in preferred littoral habitats. This may facilitate the emergence of an ideal free distribution of pike along resource gradients.     

Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish

Altered neurological function will generally be behaviourally apparent. Many of the behavioural models pioneered in mammalian models are portable to zebrafish. Tests are available to capture alterations in basic motor function, changes associated with exteroceptive and interoceptive sensory cues, and alterations in learning and memory performance. Excepting some endpoints involving learning, behavioural tests can be carried out at 4 days post fertilization. Given larvae can be reared quickly and in large numbers, and that software solutions are readily available from multiple vendors to automatically test behavioural responses in 96 larvae simultaneously, zebrafish are a potent and rapid model for screening neurological impairments. Coupling current and emerging behavioural endpoints with molecular techniques will permit and accelerate the determination of the mechanisms behind neurotoxicity and degeneration, as well as provide numerous means to test remedial drugs and other therapies. The emphasis of this review is to highlight unexplored/underutilized behavioural assays for future studies. This article is part of a Special Issue entitled Zebrafish Models of Neurological Diseases.     

Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming

Global warming is increasing the overheating risk for many organisms, though the potential for plasticity in thermal tolerance to mitigate this risk is largely unknown. In part, this shortcoming stems from a lack of knowledge about global and taxonomic patterns of variation in tolerance plasticity. To address this critical issue, we test leading hypotheses for broad-scale variation in ectotherm tolerance plasticity using a dataset that includes vertebrate and invertebrate taxa from terrestrial, freshwater and marine habitats. Contrary to expectation, plasticity in heat tolerance was unrelated to latitude or thermal seasonality. However, plasticity in cold tolerance is associated with thermal seasonality in some habitat types. In addition, aquatic taxa have approximately twice the plasticity of terrestrial taxa. Based on the observed patterns of variation in tolerance plasticity, we propose that limited potential for behavioural plasticity (i.e. behavioural thermoregulation) favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’. Finally, we find that all ectotherms have relatively low acclimation in thermal tolerance and demonstrate that overheating risk will be minimally reduced by acclimation in even the most plastic groups. Our analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures.     

The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms

Emerging evidence suggests that a group of dietary-derived phytochemicals known as flavonoids are able to induce improvements in memory, learning and cognition. Flavonoids have been shown to modulate critical neuronal signalling pathways involved in processes of memory, and therefore are likely to affect synaptic plasticity and long-term potentiation mechanisms, widely considered to provide a basis for memory. Animal dietary supplementation studies have further shown that flavonoid-rich foods are able to reverse age-related spatial memory and spatial learning impairments. A more accurate understanding of how a particular spatial memory task works and of which aspects of memory and learning can be assessed in each case, are necessary for a correct interpretation of data relating to diet-cognition experiments. Further understanding of how specific behavioural tasks relate to the functioning of hippocampal circuitry during learning processes might be also elucidative of the specific observed memory improvements. The overall goal of this review is to give an overview of how the hippocampal circuitry operates as a memory system during behavioural tasks, which we believe will provide a new insight into the underlying mechanisms of the action of flavonoids on cognition.     

Competition as a source of constraint on life history evolution in natural populations

Competition among individuals is central to our understanding of ecology and population dynamics. However, it could also have major implications for the evolution of resource-dependent life history traits (for example, growth, fecundity) that are important determinants of fitness in natural populations. This is because when competition occurs, the phenotype of each individual will be causally influenced by the phenotypes, and so the genotypes, of competitors. Theory tells us that indirect genetic effects arising from competitive interactions will give rise to the phenomenon of ‘evolutionary environmental deterioration'', and act as a source of evolutionary constraint on resource-dependent traits under natural selection. However, just how important this constraint is remains an unanswered question. This article seeks to stimulate empirical research in this area, first highlighting some patterns emerging from life history studies that are consistent with a competition-based model of evolutionary constraint, before describing several quantitative modelling strategies that could be usefully applied. A recurrent theme is that rigorous quantification of a competition''s impact on life history evolution will require an understanding of the causal pathways and behavioural processes by which genetic (co)variance structures arise. Knowledge of the G-matrix among life history traits is not, in and of itself, sufficient to identify the constraints caused by competition.