Changes in reproductive physiology and behaviour over the nesting cycle in male three‐spined sticklebacks

Plasma 11‐Ketotestosterone (11 KT) and testosterone (T) levels and spiggin‐mRNA levels, as well as the kidney‐somatic index ( I _K) were measured in sexual males and in paternal males at the middle (5 days paternal) and at the end (8 days paternal with hatched eggs) of the nesting cycle in three‐spined sticklebacks Gasterosteus aculeatus from two populations. Glueing (using threads of 11 KT induced kidney‐protein spiggin) and fanning behaviour was measured daily. Fanning increased in paternal fish and remained low in sexual males. Plasma 11 KT and T levels, on the other hand, declined significantly in parental compared to sexual males as did spiggin expression, I _K and glueing behaviour. Thus, the drastic decrease in circulating 11 KT levels during the later parental phase may have resulted in an energy‐saving decrease in spiggin‐production and glueing, when this was no longer needed for nest maintenance. In addition, the mRNA levels of the β‐subunits of both gonadotropins, luteinising hormone (LH) and follicle stimulating hormone (FSH) were measured. The expression of both gonadotropins declined in the parental phase (not significant for β‐FSH in one of the populations) which was consistent with a decline in androgen levels possibly controlled via decreased gonadotropin secretion.     

Parallel evolution of sexual isolation in sticklebacks

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.     

Changed environmental conditions weaken sexual selection in sticklebacks

Environmental heterogeneity can cause the intensity and direction of selection to vary in time and space. Yet, the effects of human-induced environmental changes on sexual selection and the expression of mating traits of native species are poorly known. Currently, the breeding habitats of the three-spined stickleback Gasterosteus aculeatus are changing in the Baltic Sea because of eutrophication and increased growth of algae. Here we show that enhanced growth of filamentous algae increases the costs of mating by inducing an increase in the time and energy spent on courtship and mate choice. This is not followed by a concomitant increase in mate attraction, but instead the strength of selection on male red nuptial coloration and courtship activity is relaxed. Thus, the high investment into the costly sexually selected traits is maladaptive under the new conditions, and the mating system mediates a negative effect of the environmental change on the population. We attribute these environmentally induced changes in the benefit of the mating traits and in the strength of sexual selection to reduced visibility in dense vegetation. Anthropogenic disturbances hence affect the selection pressures that mould the species, which could have long-term effects on the viability and evolution of the populations.     

Queen control over reproductive decisions--no sexual deception in the ant Lasius niger

Queen-worker conflicts in social insect societies have received much attention in the past decade. In many species workers modify the colony sex ratio to their own advantage or produce their own male offspring. In some other species, however, queens seem to be able to prevent workers from making selfish reproductive decisions. So far, little effort has been made to find out how queens may keep control over sex ratio and male parentage. In this study we use a Lasius niger population under apparent queen control to show that sexual deception cannot explain queen dominance in this population. The sexual deception hypothesis postulates that queens should prevent workers from discriminating against males by disguising male brood as females. Contrary to the predictions of this hypothesis, we found that workers are able to distinguish male and female larvae early in their development: in early spring workers generally placed only either female or male larvae in the uppermost chambers of the nest, although both types of larvae must have been present. At this time males were only at 11% of their final dry weight, a developmental stage at which (according to two models) workers would still have benefited from replacing queen-produced males by females or worker-produced males. This study thus demonstrates that sexual deception cannot account for the apparent queen control over colony sex ratio and male parentage in L. niger.     

Fluctuating asymmetry and reproductive isolation between two sticklebacks

This paper describes patterns of developmental asymmetry in a limnetic-benthic stickleback species pair from Paxton Lake, British Columbia. Three gill raker characters and one armor character were compared among full-sib parental crosses and their hybrids (F₁, F₂ and backcrosses). All crosses displayed asymmetry, but no differences in mean or fluctuating asymmetry were detected among laboratory-reared crosses. When wild-caught limnetics and benthics were included in the analyses significant differences in FA among groups were detected in gill raker length and plate number. The effect appears to be solely due to wild-caught benthics, though the reasons for their greater asymmetry are unknown. The patterns in laboratory-reared crosses suggest that asymmetry is unlikely to promote reproductive isolation between the parental species.     

VMHvllCckar cells dynamically control female sexual behaviors over the reproductive cycle

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Carotenoid-based sexual coloration and body condition in nesting male sticklebacks

The extent, corrected for body size, and intensity of nuptial coloration of breeding male three-spined sticklebacks Gasterosteus aculeatus L. from a Scottish freshwater population were highly variable but correlated, both in the field and after a period of nest-building in the laboratory. However, marked changes in coloration occurred between the field and the laboratory screenings and the coefficients of variation amongst males decreased. In general, intensity of coloration increased between the field and laboratory screenings, but changes in size-corrected extent were not consistently directional. For both indices, there was a negative relationship between the field value and amount by which colour changed between sampling sessions, with fish that were initially the dullest gaining most in colour. Size-corrected extent and (in particular) intensity of coloration in the field sample were associated positively with body condition measured post mortem and there was a negative, though non-significant, relationship between the extent of coloration and the proportion of white cells in the blood. No such associations were found for the laboratory colour screening. The concentration of astaxanthin in the lower jaw was related strongly and positively to both size-corrected extent and intensity of coloration at the laboratory screening and related negatively, though non-significantly, to proportional white cell counts. These data have implications both for the interpretation of previous laboratory studies and for the design of future experiments, and suggest that coloration is only a true indicator of male quality when measured in the field.     

Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females

Abstract.  The first objective of the present study is to test the hypothesis that the decrease in the number of eupyrene spermatozoa in the spermatheca is directly associated with the resumption of sexual receptivity in female moths, an aspect that has not been examined in previous studies. The obliquebanded leafroller, Choristoneura rosaceana , is used and females mated with previously mated males have a shorter refractory period than those mated with virgins. This difference is associated with a faster rate of movement of sperm from the spermatheca. Overall, the length of the female refractory period coincides with the mean time required for the number of eupyrene sperm in the spermatheca to drop to approximately 3000, regardless of male mating history. Although such a decline in sperm numbers may be a factor responsible for the resumption of sexual receptivity, this is clearly not the only one because more than 40% of females remate even though sperm numbers in the spermatheca are well above this threshold. Virgin males do not vary the mass or the content of their ejaculate as a function of the female's reproductive status and this may increase the risk of sperm competition if the female is previously mated. The second objective of this study is to examine the effect of previous male mating history on female reproductive potential. Females mated with previously mated males have a significantly lower fecundity than those mated with virgin males. However, in all treatments, remating increases both female longevity and lifetime fecundity. There is also a significant effect of female mass on the length of the refractory period and on lifetime fecundity, with large females resuming sexual receptivity sooner and laying more eggs than small ones, regardless of male mating history.     

Heterochronic expression of sexual reproductive programs during apomictic development in Tripsacum

Some angiosperms reproduce by apomixis, a natural way of cloning through seeds. Apomictic plants bypass both meiosis and egg cell fertilization, producing progeny that are genetic replicas of the mother plant. In this report, we analyze reproductive development in Tripsacum dactyloides, an apomictic relative of maize, and in experimental apomictic hybrids between maize and Tripsacum. We show that apomictic reproduction is characterized by an alteration of developmental timing of both sporogenesis and early embryo development. The absence of female meiosis in apomictic Tripsacum results from an early termination of female meiosis. Similarly, parthenogenetic development of a maternal embryo in apomicts results from precocious induction of early embryogenesis events. We also show that male meiosis in apomicts is characterized by comparable asynchronous expression of developmental stages. Apomixis thus results in an array of possible phenotypes, including wild-type sexual development. Overall, our observations suggest that apomixis in Tripsacum is a heterochronic phenotype; i.e., it relies on a deregulation of the timing of reproductive events, rather than on the alteration of a specific component of the reproductive pathway.     

Environmental enrichment,sexual dimorphism,and brain size in sticklebacks

Evidence for phenotypic plasticity in brain size and the size of different brain parts is widespread, but experimental investigations into this effect remain scarce and are usually conducted using individuals from a single population. As the costs and benefits of plasticity may differ among populations, the extent of brain plasticity may also differ from one population to another. In a common garden experiment conducted with three‐spined sticklebacks (Gasterosteus aculeatus) originating from four different populations, we investigated whether environmental enrichment (aquaria provided with structural complexity) caused an increase in the brain size or size of different brain parts compared to controls (bare aquaria). We found no evidence for a positive effect of environmental enrichment on brain size or size of different brain parts in either of the sexes in any of the populations. However, in all populations, males had larger brains than females, and the degree of sexual size dimorphism (SSD) in relative brain size ranged from 5.1 to 11.6% across the populations. Evidence was also found for genetically based differences in relative brain size among populations, as well as for plasticity in the size of different brain parts, as evidenced by consistent size differences among replicate blocks that differed in their temperature.     

No intra-locus sexual conflict over reproductive fitness or ageing in field crickets

Differences in the ways in which males and females maximize evolutionary fitness can lead to intra-locus sexual conflict in which genes delivering fitness benefits to one sex are costly when expressed in the other. Trade-offs between current reproductive effort and future reproduction and survival are fundamental to the evolutionary biology of ageing. This leads to the prediction that sex differences in the optimization of age-dependent reproductive effort may generate intra-locus sexual conflict over ageing rates. Here we test for intra-locus sexual conflict over age-dependent reproductive effort and longevity in the black field cricket, Teleogryllus commodus. Using a half-sib breeding design, we show that the most important components of male and female reproductive effort (male calling effort and the number of eggs laid by females) were positively genetically correlated, especially in early adulthood. However, the genetic relationships between longevity and reproductive effort were different for males and females, leading to low genetic covariation between male and female longevity. The apparent absence of intra-locus sexual conflict over ageing suggests that male and female longevity can evolve largely independently of one another.     

Attractive amplifiers in sexual selection: where efficacy meets honesty

How signals have evolved to convey reliable information is a major issue in the study of animal communication. The handicap principle states that recipients must impose differential costs on signallers. Here, we present an alternative hypothesis, the attractive amplifier hypothesis, according to which recipients acquire reliable information by imposing differential benefits on signallers. The attractive amplifier is a non-informative, low-cost phenotypic trait that allows recipients to increase the amount of reliable information acquired from other informative traits. We present a mating-decision model, in which mate attractiveness depends on the multiplicative-interaction between a trait that is positively correlated with mate quality and its attractive amplifier. The evaluation of both traits is assumed to be prone to error. The model shows that, to be an amplifier of cues, an attractive trait must show two well-known consequences of signal ritualization: it must be conspicuous and it must be perceived as a highly stereotyped trait, that is, it must show a low variation at both the within-individual and the within-population levels.     

Human-induced water turbidity alters selection on sexual displays in sticklebacks

Changes in the environment due to human activities are becomingincreasingly common. A serious problem in aquatic environmentsis increased water turbidity due to phytoplankton algal growth.This may affect the breeding system of fishes, especially thosewith a visually based mating system. Here we show that increasedturbidity affects sexual selection in the threespine stickleback(Gasterosteus aculeatus) through impaired possibility for visuallybased mate choice. In a laboratory mate preference and matechoice experiment on sticklebacks from the Baltic Sea, whichis an area suffering from increased turbidity due to human activities,we found that females spent more time with and visited moreoften males in clear water than males in turbid water. For malesin turbid water to receive the same amount of interest fromfemales as males in clear water, they needed to court significantlymore. Thus, turbid water induced selection for higher courtshipactivity. However, the final spawning decision of the femalesdid not depend on water turbidity, which suggests that nonvisualcues determined the final spawning decision. Because visualcues are important in mate attraction, increased turbidity affectsan important evolutionary force, sexual selection, which mayhave further consequences for the evolution of the sexual displaysand preferences. Differences in visual conditions could hencebe one factor that has lead to differences among sticklebackpopulation in the use of sexual signals.     

A comparison of the reaction of sticklebacks in different reproductive conditions towards conspecifics and predators

Experiments are described which assess ‘boldness’ towards a pike and ‘aggressiveness’ towards conspecifics in sticklebacks in non-reproductive condition, with a newly-built nest and with a recently hatched brood of young. The level of both of these aspects of behaviour increased across the three conditions. The possibility that this covariance indicates shared internal causal factors for the response to predator and conspecific is discussed.     

Analysis of the factors related with mate choice and reproductive success in male three-spined sticklebacks

Territorial three-spined sticklebacks moved 5·3 times as far as non-territorial males in 2 min ( P < 0·001) and spent 11·1 times longer in aggression in the pools ( P < 0·001). Territorial males had slightly higher condition factors than non-territorial males. Condition factor was correlated positively with the gonad mass ( P < 0·006), carotenoid concentration ( P < 0·006) and the activity of CS in the axial muscle ( P < 0·05) and lactate dehydrogenase (LDH) in pectoral muscle ( P < 0·003). The male traits best correlated positively with female mate choice were courtship effort ( P < 0·001), coloration ( P < 0·003) and initial condition ( P < 0·025). Courtship behaviour was related to intestine mass ( P < 0·018), axial ( P < 0·028) and pectoral muscle citrate synthase (CS) activity ( P < 0·047); coloration was related to gonad mass ( P < 0·037). These muscle enzymes may be involved in ATP generation for sustained activities or in recuperation between bouts of burst activity. Females that choose to mate with assiduously courting males which bear higher CS levels may be choosing individuals that show honestly their good condition and capacity to accomplish reproductive tasks.     

Long-range signalling in plant reproductive development

Animals and plants produce regulatory signals at specific places of their bodies, in order to regulate developmental events which take place at a distance. Plants use this mechanism to adjust their development to the changing environment. Flowering and tuber formation are controlled by signals generated in the leaves that travel throughout the plant to reach their target tissues: the shoot apical meristem for flowering and the underground stolons for tuberization. Although the existence of these long-distance plant messengers was postulated almost seventy years ago, their chemical nature is still not clear. These leaf-derived signals are graft-transmissible and move through the plant vascular system. Presumably they are very similar or even identical for flowering and tuberization and common to most plant species. It is generally accepted that their composition is complex and includes positive and negative regulators. Many different substances, including classical plant hormones and metabolites have been postulated to be components of these mobile signals, but conclusive evidence of this is still lacking. Recent work has positioned these signals within the genetic network that regulates flowering time and suggests roles for specific genes in the generation, transport or response to the signalling molecules. Current knowledge of long-range signalling mechanisms in other physiological and developmental events, together with the finding of common regulators involved in flowering, tuberization and other processes like pathogen and wound responses, should help to establish the biochemical composition of these elusive messenger signals.     

Purinergic signalling in the reproductive system in health and disease

There are multiple roles for purinergic signalling in both male and female reproductive organs. ATP, released as a cotransmitter with noradrenaline from sympathetic nerves, contracts smooth muscle via P2X1 receptors in vas deferens, seminal vesicles, prostate and uterus, as well as in blood vessels. Male infertility occurs in P2X1 receptor knockout mice. Both short- and long-term trophic purinergic signalling occurs in reproductive organs. Purinergic signalling is involved in hormone secretion, penile erection, sperm motility and capacitation, and mucous production. Changes in purinoceptor expression occur in pathophysiological conditions, including pre-eclampsia, cancer and pain.     

Changes in gene expression within the nucleus accumbens and striatum following sexual experience

Sexual experience, like repeated drug use, produces long-term changes including sensitization in the nucleus accumbens and dorsal striatum. To better understand the molecular mechanisms underlying the neuroadaptations following sexual experience, we employed a DNA microarray approach to identify genes differentially expressed between sexually experienced and sexually naive female hamsters within the nucleus accumbens and dorsal striatum. For 6 weeks, a stimulus male was placed in the home cage of one-half of the hormonally primed, ovariectomized female hamsters. On the seventh week, the two experimental groups were subdivided, with one half paired with a stimulus male. In comparison with sexually naive animals, sexually experienced hamsters receiving a stimulus male on week 7 exhibited an increase in a large number of genes. Conversely, sexually experienced female hamsters not receiving a stimulus male on week 7 exhibited a reduction in the expression of many genes. For directional changes and the categories of genes regulated by the experimental conditions, data were consistent across the nucleus accumbens and dorsal striatum. However, the specific genes exhibiting changes in expression were disparate. These experiments, among the first to profile genes regulated by female sexual behavior, will provide insight into the mechanisms by which both motivated behaviors and drugs of abuse induce long-term changes in the mesolimbic and nigrostriatal dopamine pathways.     

Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks

The threespine stickleback ( Gasterosteus aculeatus ) species complex is well suited for identifying the types of phenotypic divergence and isolating barriers that contribute to reproductive isolation at early stages of speciation. In the present study, we characterize the patterns of genetic and phenotypic divergence as well as the types of isolating barriers that are present between two sympatric pairs of threespine sticklebacks in Hokkaido, Japan. One sympatric pair consists of an anadromous and a resident freshwater form and shows divergence in body size between the forms, despite the lack of genetic differentiation between them. The second sympatric pair consists of two anadromous forms, which originated before the last glacial period and are currently reproductively isolated. These two anadromous forms have diverged in many morphological traits as well as in their reproductive behaviours. Both sexual isolation and hybrid male sterility contribute to reproductive isolation between the anadromous species pair. We discuss the shared and unique aspects of phenotypic divergence and reproductive isolation in the Japanese sympatric pairs compared with postglacial stickleback species pairs. Further studies of these divergent species pairs will provide a deeper understanding of the mechanisms of speciation in sticklebacks.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 671–685.