Theory of resource allocation strategy in territorial male tropical reef fishes

A mathematical model is proposed to explain energy resource allocation between sperm production and territoriality in male reef fishes (Labridae species) from the point of view of optimization. Labridae species are typically characterized by both TP (terminal phase) and IP (initial phase) males. The former are considered to release a lower amount of sperm but show aggressive territoriality. In the model, TP male reproductive success is considered as depending upon both fertilization probability (depending on sperm density) and the individual's own territorial activities. Between these factors, a trade-off exists by which the fertilization probability can be enhanced only by reducing territoriality. Therefore, the male has to decide how much of the total available energy resource should be allocated to each. The model showed that under high fertilization efficiency the male can achieve high success by spending less of the resource on sperm production and correspondingly more for territoriality. The TP male reproductive success increases with decreasing male density in the habitat. Nevertheless, when intruding males cannot be excluded completely by territorial behavior of the TP male, females prefer high male density. If females can control the number of intruding males to some degree, conflict may arise between the sexes. Received: December 8, 1999 / Accepted: May 24, 2000     

The evolution of parental care in shorebirds: life histories, ecology, and sexual selection

Parental care is expected to evolve according to a trade-offbetween the benefits of increased survival of offspring andcosts of reduced survival and future reproduction of adults.Here we investigate the components of this life-history trade-offin shorebirds (Charadriides, excluding Laroidea), an avian infraorderdisplaying an unusual diversity in extent of care by each sex.We show that evolutionary increases in the duration of carein one sex are associated with decreased care by the other.We found no evidence that various hypothesised benefits of careprovide a general explanation for the duration of care by eitheror both sexes, although parental feeding of the young was tooconservative for comparisons. Sexual dimorphism in body sizehad a similar relationship to parental care in both sexes: reductionsin duration of care by either sex were matched by increasesin the size of that sex relative to the other. Whereas thispattern could be explained by sexual selection in males, itwas retained within socially monogamous females. Reduced carein males (but not in females) appears to have facilitated theevolution of greater migration distances. These results suggestthat parental care has had different causes and consequencesin each sex. Benefits of desertion due to sexual selection aremore clearly demonstrable for males, whereas correlates of careare less clear for females     

Fishes as models in studies of sexual selection and parental care

Fishes are by far the most diverse group of vertebrates. This fact is in no way, however, reflected in their use as model organisms for understanding sexual selection or parental care. Why is this so? Is it because fishes are actually poor models? The usefulness of fishes as models for sexual selection and parental care is discussed by emphasizing some problems inherent in fish studies, along with a number of reasons why fishes are indeed excellently suited. The pros and cons of fishes as models are discussed mainly by comparison with birds, the most popular model organisms in animal behaviour. Difficulties include a lack of background knowledge for many species, and the problems of marking and observing fishes in their natural environment. Positive attributes include the diversity of lifestyles among fishes, and the ease with which they can be studied experimentally in the laboratory. How useful fish models can be is briefly illustrated by the impressive and broadly relevant advances derived from studies of guppies Poecilia reticulata and three‐spined sticklebacks Gasterosteus aculeatus . A selection of topics is highlighted where fish studies have either advanced or could greatly enhance, the understanding of processes fundamental to animal reproductive dynamics. Such topics include sex role dynamics, the evolution of female ornamentation and mate choice copying. Finally, a number of potential pitfalls in the future use of fish as models for sexual selection and parental care are discussed. Researchers interested in these issues are recommended to make much more extensive use of fish models, but also to adopt a wider range of models among fishes.     

The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory

Males and females are often defined by differences in their energetic investment in gametes. In most sexual species, females produce few large ova, whereas males produce many tiny sperm. This difference in initial parental investment is presumed to exert a fundamental influence on sex differences in mating and parental behavior, resulting in a taxonomic bias toward parental care in females and away from parental care in males. In this article, we reexamine the logic of this argument as well as the evolutionarily stable strategy (ESS) theory often used to substantiate it. We show that the classic ESS model, which contrasts parental care with offspring desertion, violates the necessary relationship between mean male and female fitness. When the constraint of equal male and female mean fitness is correctly incorporated into the ESS model, its results are congruent with those of evolutionary genetic theory for the evolution of genes with direct and indirect effects. Male parental care evolves whenever half the magnitude of the indirect effect of paternal care on offspring viability exceeds the direct effect of additional mating success gained by desertion. When the converse is true, desertion invades and spreads. In the absence of a genetic correlation between the sexes, the evolution of paternal care is independent of maternal care. Theories based on sex differences in gametic investment make no such specific predictions. We discuss whether inferences about the evolution of sex differences in parental care can hold if the ESS theory on which they are based contains internal contradictions.     

The evolution of male infanticide in relation to sexual selection in mammalian carnivores

The evolution of infanticide by males has often been explained by the sexual selection hypothesis, which posits that infanticide improves male reproductive success by shortening the interbirth intervals of the mothers of the killed offspring. In Carnivora, however, the fitness advantages assumed in this hypothesis have been shown in only a few species, and it has been argued that male infanticide may be nonadaptive in pinniped carnivores. According to the sexual selection hypothesis, male infanticide is expected to be more prevalent in species in which males are subjected to stronger sexual selection through intrasexual competition over mates. We examined a phylogenetically corrected relationship between male infanticide and sexual size dimorphism (SSD) as a measure of the intensity of sexual selection in carnivores. Our analyses failed to detect a significant association between the occurrence of male infanticide and SSD across carnivores, although they showed that, among fissipeds (typically terrestrial carnivores), males in species with stronger male-biased SSD are significantly more likely to commit infanticide. This suggests that the evolution of male infanticide is correlated with intense sexual selection in fissipeds. In pinnipeds (Odobenidae, Otariidae, and Phocidae), there was no significant association between male infanticide and SSD. Assuming that SSD represents the intensity of sexual selection on males, this result is consistent with the argument that infanticide by male pinnipeds is not a sexually selected behaviour.     

Pre- and postnatal bisphenol A treatment results in persistent deficits in the sexual behavior of male rats, but not female rats, in adulthood

Perinatal administration of the endocrine disruptor bisphenol A (BPA) reportedly inhibits the sexual behavior of sexually naïve adult male rats. In order to evaluate the effects of BPA administration during early development on later reproductive behavior, we administered one of five doses of bisphenol A daily to pregnant female rats throughout gestation and lactation, and quantified the appetitive and consummatory sexual behaviors of the resultant male and female offspring over multiple sexual encounters in adulthood. Males receiving low dose perinatal BPA (50 μg/kg bw/day) showed persistent deficits in sexual behavior in adulthood. Males receiving the highest dose (5 mg/kg bw/day), however, were indistinguishable from controls with respect to consummatory sexual behaviors but showed decreased latencies to engage in those behaviors when sexually naïve, with significant non-linear, or U-shaped, dose-response relationships observed on the first and last day of testing. Adult female sexual behavior was not affected by early BPA administration at any dose tested. These results are consistent with previous reports that BPA exerts behavioral effects especially at low doses, and further indicates that BPA can cause lasting impairment of sexual behavior in males, but does not alter the normal development of female appetitive or consummatory sexual behaviors. To our knowledge, this is the first report indicating that adult sexual performance is impaired in sexually experienced animals following perinatal exposure to bisphenol A.     

The evolution of migration and some life history parameters in marine fishes

Synopsis Migration is a common phenomenon in marine fishes but the consequences with respect to life history variation have been little explored. Migration both influences the evolution of other traits and is contigent upon the evolution of other behavioural and demographic characters. The interaction between such factors is illustrated by considering the relationship between the cost of migration in relation to fecundity and the advantages and disadvantages of schooling, a phenomenon hypothesized to favour the evolution of migration. These analyses predict that migratory species will be relatively large, mature late and at a relatively large size and grow relatively fast. Data from north temperate marine fish support these predictions.     

The behavioral ecology of three Indian Ocean surgeonfishes (Acanthurus lineatus,A. leucosternon and Zebrasoma scopas): their feeding strategies,and social and mating systems

Synopsis The relationship between the morphology, feeding strategies and social and mating systems of three surgeonfishes was investigated. Adults of each defend feeding territories, intra-and interspecifically. The largest species, because of its morphological limitation, relies on food that has to be defended against many other species. It forms large colonies in which fishes singly defend small territories containing high standing crop algal mats. Colony formation is a mechanism by which the efficiency and effectiveness of interspecific territory defense is increased. The smallest species, because of its morphological adaptations, is able to rely most on food that other species cannot efficiently exploit. It forms pairs that defend large territories containing a thin algal mat. It is restricted to the poorest quality habitat by the aggressive activities of more dominant species. The third species, which also forms pairs, has an intermediate feeding strategy. The local coexistence of these three and other surgeonfishes results from a combination of (i) their partitioning both habitat and food resources, and (ii) the populations of two of the most dominant species apparently being below the carrying capacity. Territoriality and the absence of parental care facilitates pair formation in surgeonfishes. Permanently territorial species usually form pairs. The colonial species does not form pairs because the colonial habit facilitates interference of males in each other's spawnings.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

The evolution of parental care in freshwater leeches

Summary The life-history strategies of a selection of the most common European freshwater leeches (Euhirudinea) are described. On the basis of this information and results from the literature, the probable phylogenetic development of parental care in the Euhirudinea is reconstructed. The jawless worm leeches (Erpobdellidae) secrete a protective cocoon, cement it to the substrate and sometimes ventilate it before they leave the egg capsules. This behaviour represents the most ancient state in leech evolution. Members of the jawed Hirudinidae deposit desiccation-resistant cocoons on land. All known Glossiphoniidae (leeches equipped with a proboscis) have evolved the habit of brooding the eggs and young. These unique parental care patterns within one family of extant freshwater leeches can be arranged schematically in a series of increasing complexity which may reflect the evolution of brooding behaviour. Glossiphoniid leeches of the genus Helobdella, which have a world-wide distribution, display the most highly developed parental care system: they not only protect but also feed the young they carry. This results in the young being much larger when they leave the parent and, presumably, in higher subsequent survival. Isolated cocoons of all aquatic leeches are rapidly destroyed by predators, primarily water snails. In erpobdellids (but not glossiphoniids, which protect the cocoons) a large portion of the cocoons are lost due to predatory attacks. We conclude that the major selective pressure driving the evolution of parental care in leeches may have been predation on eggs and juvenile stages. Dedicated to Professor Dr. G. Osche on the occasion of his 75th birthday     

The intensity of sexual selection in relation to male sexual behaviour,female choice,and sperm precedence

In this paper we define sexual selection on males as the variance in numbers of mates per male and show how the intensity of this selection is affected by male sexual behaviour, female choice, sex ratio, and modes of sperm precedence. This definition coincides with Darwin's conception of sexual selection but differs from some post-Darwinian views. For systems of single-male paternity, we show that the intensity of total selection on male reproductive success equals the intensity of natural selection on female fertility, times the sex ratio, plus the intensity of sexual selection on males. The absolute intensity of sexual selection is unaffected by the system of sperm precedence. The application of the results to field studies is discussed.     

The opportunity to be misled in studies of sexual selection

It is a challenge to measure sexual selection because both stochastic events (chance) and deterministic factors (selection) generate variation in individuals' reproductive success. Most researchers realize that random events ('noise') make it difficult to detect a relationship between a trait and mating success (i.e. the presence of sexual selection). There is, however, less appreciation of the dangers that arise if stochastic events vary systematically. Systematic variation makes variance-based approaches to measuring the role of selection problematic. This is why measuring the opportunity for sexual selection (I(s) and I(mates)) is so vulnerable to misinterpretation. Although I(s) does not measure actual sexual selection (because it includes stochastic variation in mating/fertilization success) it is often implicitly assumed that it will be correlated with the actual strength of sexual selection. The hidden assumption is that random noise is randomly distributed across populations, species or the sexes. Here we present a simple numerical example showing why this practice is worrisome. Specifically, we show that chance variation in mating success is higher when there are fewer potential mates per individual of the focal sex [i.e. when the operational sex ratio (OSR), is more biased]. This will lead to the OSR covarying with I(s) even when the strength of sexual selection is unaffected by the OSR. This can generate false confidence in identifying factors that determine variation in the strength of sexual selection. We emphasize that in nature, even when sexual selection is strong, chance variation in mating success is still inevitable because the number of mates per individual is a discrete number. We hope that our worked example will clarify a recent debate about how best to measure sexual selection.     

Termination of parental care due to small clutch size in the temperate damselfish,Chromis notata

Synopsis Reproductive behavior of the temperate damselfish, Chromis notata, was investigated on the island of Mukaishima, Japan, almost daily during the breeding season in 1982. Both males and females repeated reproductive cycles many times during the breeding season. Females had a strong tendency to spawn a whole clutch on one nest during a few hours. The average number of eggs which a male gained per reproductive cycle was estimated at 38560 (480–131100 eggs). Males ordinarily cared for eggs until just prior to hatching, but abandoned more than half of the nests with the eggs numbering less than 11568. Contribution 207 from the Mukaishima Marine Biological Station.     

The nest-holding grass goby (Zosterisessor ophiocephalus) male adjusts the spawning activity in relation to parasitic nest intrusions

This study examines the temporal pattern of spawning behavior by the territorial (i.e. nest-holding) grass goby male, Zosterisessor ophiocephalus, in response to sneak intrusions by the small parasitic male under controlled laboratory conditions. The spawning activity of the territorial male consists of a sequence of upside–down movements on the ceiling of the nest accompanied by undulations of the body and sperm release. Five pairs of one territorial male and one parasitic male, each kept inside a large tank provided with an artificial buried nest (always occupied by the territorial male) and one small tunnel-shaped shelter (always occupied by the small male), were observed during one-female spawning taking place in the innermost part of the nest (i.e. the nest chamber). During the spawning, the presence of the small male nearby the nest openings elicited aggressive behavior and increased nest patrolling by the territorial male. In one spawn the small male never attempted to enter the nest. In four spawns the small male entered one to three times the nest chamber (sneaks), staying there from 2 to 203 s until the large male chased him away. The temporal patterning of the spawning activity by the territorial male (bouts of upside–down, U–D), and its changes following a sneak by the small male, were investigated using bout analysis and correlative tests. Results showed the length of bouts U–D did not change significantly after a sneak intrusion. whereas gap length (i.e. the period between subsequent bouts U–D) decreased significantly after each sneak intrusion. The mean duty cycle of bouts U–D tended to be positively correlated to the number of sneaker intrusions of each replicate. Results are discussed in the light of current knowledge on sperm competition among externally fertilizing teleosts.     

昆虫性选择行为研究进展

本文综述了昆虫的各种性选择行为,包括与个体大小有关的性选择行为、与鸣声有关的性选择行为、与“婚礼食物”有关的性选择行为以及精子竞争等。     

The evolution of complex brains and behaviors in African cichlid fishes

In this review, I explore the effects of both social organization and the physical environment, specifically habitat complexity, on the brains and behavior of highly visual African cichlid fishes, drawing on examples from primates and birds where appropriate. In closely related fishes from the monophyletic Ectodinii clade of Lake Tanganyika, both forces influence cichlid brains and behavior. Considering social influences first, visual acuity differs with respect to social organization (monogamy versus polygyny). Both the telencephalon and amygdalar homologue, area Dm, are larger in monogamous species. Monogamous species are found to have more vasotocin-immunoreactive cells in the preoptic area of the brain. Habitat complexity also influences brain and behavior in these fishes. Total brain size, telencephalic and cerebellar size are positively correlated with habitat complexity. Visual acuity and spatial memory are enhanced in cichlids living in more complex environments. However habitat complexity and social forces affect cichlid brains differently. Taken together, our field data and plasticity data suggest that some of the species-specific neural effects of habitat complexity could be the consequence of the corresponding social correlates. Environmental forces, however, exert a broader effect on brain structures than social ones do, suggesting allometric expansion of the brain structures in concert with brain size and/or co-evolution of these structures [Current Zoology 56 (1): 144-156 2010].     

Localization of monoamines in the forebrain of two salmonid species,with special reference to the hypothalamo-hypophysial system

Summary In the salmon and trout aminergic cell bodies were found in the nucleus recessus lateraralis (NRL) and the nucleus recessus posterioris (NRP), both of which are situated near the third ventricle. Three cell types could be distinguished. Type 1 produces a green and type 2 a yellow fluorescence. The former type probably contains dopamine and the latter 5-hydroxytryptamine. Both types possess intraventricular protrusions in contact with the cerebrospinal fluid. The third cell type produces a less intense blue-green fluorescence; relatively few cells of this type have thick processes in contact with the ventricle. In addition, large fluorescent cells were found in the salmon, dorsal from the caudal part of the NRL. The various parts of the NRL and NRP are interconnected by thick bundles of nerve fibers; tracts leaving the nuclei could be traced for short distances only. The cells of the nucleus praeopticus (NPO), those of the medial part and to a much lesser extent also of the lateral part of the nucleus lateralis tuberis (NLT) have an aminergic innervation which probably originates from the NRL and/or NRP. All parts of the neurohypophysis contain many monoaminergic fibers, with aminergic material concentrated at the neuro-adenohypophysial interface. Fibers were not observed to penetrate the basal lamina. In the salmon and trout the fibers have a similar distribution, but differ in the intensity of fluorescence, being high in the salmon and low in the trout. Only in the trout have fluorescent cells been found in the adenohypophysis and very occasionally in the neurohypophysis. A number of these cells are basophilic and show a PAS-positive reaction.     

Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes

Evolutionary theory predicts that sexual selection may increase taxonomic diversity when emergent mating preferences result in reproductive isolation and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P=0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis.