Effect of larval food stress on male adult behaviour, morphology and reproductive investment in the butterfly Pararge aegeria

Males of several animals increase their reproductive success by territorial behaviour. In butterflies, males may defend a territory (i.e., territorial perching tactic), but this is assumed to be an energetically costly way to locate mates. Limitations of the energy budget may affect fight performance, and may, consequently, force males to adopt an alternative non-territorial searching behaviour (i.e., patrolling tactic) to maximize reproductive success. In this study, we tested to what extent behavioural tactics adopted by adult males of the butterfly Pararge aegeria (L.) were affected by the nutritional conditions during the larval stage. We compared the occurrence of territorial versus patrolling behaviour, lipid mass, flight muscle ratio, metabolic rate and spermatophore production of low quality males that were reared as a larva on drought-stressed host plants and control, high quality males. Low quality males were less likely to adopt the territorial perching tactic and emerged as adults with lower lipid mass than high quality males, but they were able to restore their lipid mass through adult feeding (and perhaps the breakdown of flight muscles). Host plant quality also affected spermatophore size. Independent of the larval food treatment, territorial perching males metabolised more lipids than non-territorial males, produced larger spermatophores and copulated for longer than males adopting non-territorial behaviour. We discuss the results relative to the co-existence of the behavioural tactics (perching and patrolling).     

Behavior of males in a reproductive aggregation of the banded demoiselle Calopteryx splendens (Insecta, Odonata)

The view according to which damselfly males practice two alternative reproductive tactics of access to females is critically discussed. It is widely accepted that some males (“territorial” ones) have priority as potential female partners, while others (“sneakers” or “wanderers”) are incapable of retaining an individual territory. They have a chance of mating only by intruding briefly into the area defended by a “territorial” male when a female is present there. Thus, the tactics of a “territorial” male consists in waiting for a female in its territory and copulating with it “by agreement,” whereas non-territorial males resort to forced copulations. By observation of individually marked males (48 out of 118) it was shown that every male could be regarded as “territorial” during a certain period and as a “wanderer” before and after it. Thus, no correlation between the modes of space use by a male (residence/mobility) and the characters of its external morphology and/or signal behavior appears to be possible in principle. According to the data obtained, a more plausible explanation is that the female chooses not the male but the best area for oviposition. In addition, it was ascertained that adherence to forced copulations cannot constitute successful “tactics” since they rarely result in insemination, neither by “territorial” nor “non-territorial” males. In other words, we are dealing not with certain alternative tactics (i.e., specialized adaptive mechanisms that have evolved in the species) but simply with the results of different sets of circumstances at a given moment.     

Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio

Background

We used behavioural and genetic data to investigate the effects of density on male reproductive success in the zebrafish, Danio rerio. Based on previous measurements of aggression and courtship behaviour by territorial males, we predicted that they would sire more offspring than non-territorial males.

Results

Microsatellite analysis of paternity showed that at low densities territorial males had higher reproductive success than non-territorial males. However, at high density territorial males were no more successful than non-territorials and the sex difference in the opportunity for sexual selection, based on the parameter I _mates, was low.

Conclusion

Male zebrafish exhibit two distinct mating tactics; territoriality and active pursuit of females. Male reproductive success is density dependent and the opportunity for sexual selection appears to be weak in this species.     

Age-specific survival of territorial and non-territorial male chamois

How alternative reproductive tactics (ARTs) are maintained in wildlife populations is one of the major questions in evolutionary biology. As a dominant status, territoriality is typically linked to increased mating opportunities, and one explanation why this behaviour coexists with other tactics is that dominance implies survival costs. Such a trade-off may occur in the Northern chamois Rupicapra rupicapra, as reproductive advantages of territorial males over non-territorial males could be counterbalanced by a reduction in survival mediated through energy expenditure, stress and parasitic infections, ultimately favouring ART coexistence. Here, we analysed age-dependent survival probabilities of territorial (n = 15) and non-territorial (n = 16) adult chamois using information collected over 12 years between 2010 and 2021 in the Gran Paradiso National Park (Western Italian Alps). Survival rates were estimated with a CMR approach using Burnham's joint modelling of live encounter and dead recovery data. The model selection procedure, based on AICc value minimisation, supported a linear decrease of survival with age but the results did not match our predictions, as territorial chamois did not have lower survival rates than non-territorial chamois. In contrast, territorial males appeared to enjoy reproductive success at lower survival costs. This, in turn, supports the role of other factors, such as snow-dependent environmental stochasticity, in the maintenance of ARTs in chamois populations. The limited sample size, however, calls for caution in interpretation, and long-term studies of lifetime reproductive success and survival are necessary to clarify the mechanisms underlying the expression and coexistence of different reproductive behaviours in this species.     

A multidisciplinary study on social status and the relationship between inter-individual variation in hormone levels and agonistic behavior in a Neotropical cichlid fish

Social animals with hierarchal dominance systems are particularly susceptible to their social environment. There, interactions with conspecifics and hierarchal position can greatly affect an individual's behavior, physiology and reproductive success. Our experimental model, Cichlasoma dimerus, is a serially-monogamous Neotropical cichlid fish with a hierarchical social system, established and sustained through agonistic interactions. In this work, we aimed to describe C. dimerus social structure and its association with hormonal profiles and testicular cellular composition. We recorded and quantified agonistic interactions from the territorial pair, i.e. the top ranked male and female, and the lowest ranked male of stable social groups. Plasma levels of 11-ketotestosterone (11-KT), testosterone, 17β-estradiol (E₂) and cortisol were measured by ELISA. Results show that territorial pairs cooperatively guarded the territory, but rarely attacked in synchrony. Territorial males had higher testosterone and 11-KT plasma levels than non-territorial males, while E₂ and an index of its metabolization from testosterone were higher in non-territorial males. No difference was observed in cortisol levels. Plasma 11-KT and an index of the conversion of testosterone to 11-KT, positively correlated with the frequency of aggressiveness, while E₂ showed the opposite pattern. Territorial males had a higher gonadosomatic index than non-territorial males. The quantification of testicular cellular types revealed that the percentage of spermatocytes and spermatids was higher in non-territorial males, while territorial males showed a greater percentage of spermatozoa. Thus, C. dimerus male social position within a stable hierarchy is associated with distinct behaviors, steroid levels and testicular degree of development.     

Histomorphology of preorbital gland in territorial and non-territorial male blackbuck Antelope cervicapra, a critically endangered species

The preorbital gland is a specialized dermal gland of antelopes which plays an important role in territorial marking behavior and pheromonal communication. To our knowledge, there is little information available on the role of preorbital gland marks in Indian antelopes (blackbucks). Males are seen averting the gland during behavioural display and territorial marking but the functional aspect of this gland has not been examined. Hence, the aim of this study was to describe the histomorphology of the preorbital gland in territorial and non-territorial male blackbucks to determine its morphology and secretory function. The results showed that the preorbital gland is composed of modified sebaceous and apocrine glands. The apocrine gland is lined by simple cuboidal epithelial cells; the serous parts of the secretory products are often seen in the apical portions of the cells. The myoepithelial cells contain actin filaments lying on the basal membranes of the apocrine gland. There are some considerable histological changes in the presence of the sebaceous and apocrine glands in territorial males in comparison to non-territorial males. The following histological changes associated with occurrence of the sebaceous and apocrine glands have been observed in territorial and non-territorial male blackbucks: (1) increase of size of sebaceous and apocrine glands and (2) increase in density of sebaceous and apocrine glands in territorial males compared to non-territorial males. It is suggested that the higher development (i.e., size) and density of sebaceous and apocrine glands in territorial males could depend on hormone production (i.e., testosterone). Based on the histological observation and the role of sebaceous and apocrine glands in the preorbital gland supported by literature, it is possible to conclude that both territorial and non-territorial blackbuck males may produce pheromonal substances through preorbital gland (secretion) for olfactory communication.     

Variations of space use in males of the banded demoiselle (<Emphasis Type="Italic">Calopteryx splendens</Emphasis>, Zygoptera,Odonata): Alternative tactics or an age-dependent trend?

Two spatial tactics are usually distinguished in males of Calopteryx damselflies: territorial and nonterritorial. These tactics are believed to underlie two alternative condition-dependent reproductive tactics in these insects, and territorial males are believed to copulate more often. With age, males become weaker, turn nonterritorial, and only occasionally manage to copulate. However, the details of space use by damselflies are poorly known, which hinders the interpretation of the existing empirical data. We describe the space use by individually marked males of the banded demoiselle C. splendens studied during three field seasons in Vladimir Province, Russia. Each male on each day of observations was characterized as either territorial or non-territorial, and the sites of encounter were mapped. The probability of being territorial declined with the male’s age. The spatial tactics (territorial vs. non-territorial) on a given day strongly influenced the tactics used on the following day. We identified the territorial and non-territorial phases in the life of a male damselfly, which occurred consecutively and had a roughly similar duration. During the territorial phase, the male occupied a certain territory and tried to hold it as long as possible. The male abandoned its territory in two cases: (1) when it was driven onto a different territory as the result of competition with other males, or (2) when it was exhausted and became non-territorial. Thus, the space use by the male changed predictably during its life. Therefore, direct comparison of morphological or other characteristics in territorial vs. non-territorial males, frequently made in the literature, makes little sense. Further progress in studying the so-called “alternative reproductive tactics” in damselflies may be more successfully achieved by comparing individual life trajectories of different males (e.g. duration of territorial and non-territorial periods, the number of consecutively occupied territories, etc.). We performed correlation analysis and found that the above parameters did not depend on the wing and abdomen length of the males.     

Reproductive success in male Japanese minnows,Pseudorasbora parva: observations under experimental conditions

To evaluate the spawning success of male Japanese minnows,Pseudorasbora parva, and female mate choice, spawning behaviour was observed under both artificial and experimental conditions. Larger males had larger territories and greater reproductive success. The body weight of territorial males decreased during the maintenance of territories, while that of non-territorial males increased significantly. When the weight of non-territorial males exceeded that of territorial males, the former began to establish new territories on the substrate, suggesting a conditional strategy by non-territorial males to trade off immediate reproductive success with growth and hence improve future reproductive success. Females chose males with larger body size, probably based on dominance rank rather than the quality (or size) of territory. It was concluded that females choose males of higher dominance rank and that males compete for large territories, both of which play an important part in male reproductive success.     

Male dimorphism, territoriality and mating success in the tropical damselfly, Paraphlebia zoe Selys (Odonata: Megapodagrionidae)

The tropical damselfly Paraphlebia zoe has two male morphs: a black-winged (BW) male which is associated with territorial defense of oviposition sites; and a hyaline-winged (HW) male similar in appearance to females, and, compared to the black morph, less frequently found defending territories. In a wild population of this species, we first assessed the relationship between phenotypic traits [male morph, size and territorial status (being territorial or non-territorial)], their role on mating success, and the degree to which a particular territory may contribute to male mating success. Second, to relate a physiological basis of being territorial we compared both morphs in terms of muscular fat reserves and thoracic muscle, two key traits related to territory defense ability. Males of both morphs defended territories although the BW males were more commonly found doing this. BW males were larger than HW males and size predicted being territorial but only within HW males (territorial males were larger) but not in BW males. Male mating success was related to territorial status (territorial males achieved a higher mating success), but not to morph or size. Furthermore, territory identity also explained mating success with some territories producing more matings than others. The BW morph stored more fat reserves which may explain why this morph was more likely to secure and defend a place than the HW morph. However, the HW morph showed higher relative muscle mass which we have interpreted as a flexible strategy to enable males to defend a territory. These results are distant to what has been found in another male dimorphic damselfly, Mnais pruinosa, where the advantage of the non-territorial morph relies on its longevity to compensate in mating benefits compared to the territorial morph.     

Male Parasitic Spawning in Two Species of Triplefin Blenny (Tripterigiidae): Contrasts in Demography, Behaviour and Gonadal Characteristics

Axoclinus nigricaudus and A. carminalis are blennioid fishes from the Gulf of California, Mexico. Males show alternative mating tactics; territorial individuals attract females while non-territorial individuals parasitically spawn with territorial males' females. Demography and gonadal characteristics were related to the degree of parasitic spawning (sperm competition) within and between species. Males of both species showed bimodal size distributions that largely reflected the two tactics. Territorial males spawned much more frequently than non-territorial males, but parasitic spawning was significant. Non-territorial males were more common and rates of parasitic spawning were much higher in A. nigricaudus indicating that it experienced higher sperm competition. In agreement with sperm competition theory, relative testis weight was greater in A. nigricaudus. In A. nigricaudus, the majority of parasitic matings were by non-territorial males, whereas in A. carminalis, both male-types parasitised frequently. Accordingly, only in A. nigricaudus did non-territorial males have relatively heavier testis than territorial males. In both species the testicular gland, that produces accessory products for sperm transfer, was large in territorial males, but small or undeveloped in non-territorial males suggesting male-types differ in fertilisation mode.     

Does part reproductive history predict competitive interactions and male mating success in pupfish?

Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males' ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating success than PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success. Only males in good physical condition achieve high mating success, and both intra- and inter-sexual selection are important in maintaining the close correlation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females.     

Aggressive Transition between Alternative Male Social Tactics in a Long-Lived Australian Dragon (Physignathus lesueurii) Living at High Density

Theory predicts the evolution of alternative male social tactics when intense competition coupled with the superior competitive ability of some individuals limits access to reproductive opportunities by others. How selection has shaped alternative social tactics may be especially interesting in long-lived species where size among sexually mature males varies markedly. We conducted experimental studies on long-lived eastern Australian water dragons living where competition was intense to test the hypotheses that mature males adopt alternative social tactics that are plastic, and that large size and body condition determine resource-holding potential. Approximately one-half of mature males (N = 14) defended territories using high rates of patrol and advertisement display, whereas 16 smaller mature males having lower body condition indices utilized non-territorial social tactics. Although territorial males were larger in absolute size and head dimensions, their heads were not allometrically larger. Territorial males advertised very frequently using displays involving stereotypical movements of the head and dewlap. More aggressive displays were given infrequently during baseline social conditions, but increased during periods of social instability. Female home ranges overlapped those of several territorial and non-territorial males, but females interacted more frequently with territorial males. The extreme plasticity of social tactics in this species that are dependent on body size was confirmed by two instances when relatively large non-territorial males spontaneously evicted territory owners, and by marked shifts in tactics by non-territorial males in response to temporary experimental removals of territory owners, followed (usually) by their expulsion when original owners were reinstated. The high level of social plasticity in this population where same-sex competitors are densely concentrated in preferred habitat suggests that chronic high energetic costs of defense may select for males to cycle between territorial and non-territorial social tactics depending upon their changing energetic status and their current capacity for competition with rivals.     

Life History Dependent Behavioural Variation in Water Striders,Aquarius remigis

We investigated behavioural consequences of life history states in Aquarius (Gerris) remigis, a hemipteran surface predator and scavenger of small North American streams. A repeated-measures field study comparing reproductive and non-reproductive first summer generation females and males during the same time in summer showed that non-reproductive males and females, which were foraging to survive the winter, behaved essentially alike, often being territorial. In contrast, reproductives of both sexes were more mobile than non-reproductives, reproductive males being much more mobile than reproductive females, always in search of and attacking potential mates. This resulted in reproductive males showing litde territoriality and having lower foraging success than all other categories, while reproductive females had higher foraging success than non-reproductive females or males, thus likely increasing their fecundity. Many behavioural variables did not change with time. Exceptions were a decrease in the mating activity of reproductives of both sexes, the number of mating attempts, mobility, and the stride rate of reproductive males, and an increase in overall foraging activity of all individuals. This indicates that the behaviour of reproductive males converged towards that of non-reproductive males as the season progressed. Individuals were assigned to either state post-hoc according to whether they had been seen mating at least once during the study period (July and August). Females were further tested to ascertain if they laid eggs. These results support the hypothesis that diapause and reproductive state to some degree predetermine behaviour, thus constraining behavioural flexibility. Attributing behavioural variation to various proximate causes can be central to the interpretation of alternative strategies and tactics.     

Do Feeding Resources Induce the Adoption of Resource Defence Polygyny in a Lekking Butterfly?

Among polygynous species, males often compete for the possession of mating sites to increase their reproductive success. Weaker individuals frequently adopt alternative non‐territorial mate‐locating tactics, but the adoption of alternative territorial tactics may also occur. Although alternative tactics with territory defence are less common in arthropods, factors that drive its adoption may provide information to understand the organization of different territorial mating systems in the group. Here we investigate the adoption of resource‐based territoriality as an alternative to a non‐resource‐based one by males of the butterfly Paryphthimoides phronius. Male P. phronius commonly defend sunny clearings lacking feeding resources in the forest edge (non‐resource‐based territoriality). However, after experimentally offering fermenting fruit in previously undefended sites, we showed that males also adopt a resource defence tactic. Males in territories with fermenting fruits apparently feed on this resource when they are not defending the territory. However, males in sites without resources did not migrate to territories with resources when given the opportunity. To our knowledge, this is the first experimental investigation to show a non‐resource‐ and an alternative resource‐based mate‐locating tactic in a butterfly. We suggest that this behavioural flexibility may represent an important step to understand the ecological factors responsible for the organization and evolution of different territorial mating systems in insects.     

To be or not to be? Mating success and survival trade‐offs when switching between alternative reproductive tactics

Hormones underlie the decision of assuming a territorial or a nonterritorial role, with territorial individuals usually having higher hormonal levels than nonterritorial individuals. As a territorial status is linked to higher mating opportunities, it is unclear why animals do not keep high hormonal levels and one explanation is that this would imply survival costs. We have tested this using males of the territorial damselfly Argia emma in the field. We increased juvenile hormone (JH) levels using methoprene in both territorial and nonterritorial males and predicted that: (i) males will keep (the case of territorial males) or become (the case of nonterritorial males) territorial after hormonal increase, and (ii) there will be an increase in mating success for nonterritorial males only and an impaired survival for both male tactics. Hormonally treated males remained or became territorial but had their survival impaired compared with control groups. Also, hormonally treated, ex‐nonterritorial males increased their mating success compared with the other control, nonterritorial males. The reduced survival can be explained proximally by the energy devoted either to the enhanced aggression showed during territory defence or immune function (as detected previously in damselflies). Although nonterritorial males may increase their mating success by switching to a territorial tactic, they are possibly unable to do it naturally as JH is dietary dependent and usually nonterritorial animals are in poorer condition than territorial animals.     

A selective trade-off for territoriality and non-territoriality in the polymorphic damselfly Mnais costalis

Males of the damselfly Mnais costalis occur as territorial orange-winged 'fighter' males or non-territorial clear-winged 'sneaker' males. Their morph life histories differ considerably but the estimated lifetime reproductive success is the same for the two morphs. In this study we compared the developmental and reproductive costs associated with the two morphs. Orange-winged male and female reproductive costs resulted in a decline in adult fat reserves with increasing age. In contrast, the fat reserves of clear-winged males remained constant with adult age. Body size was positively correlated with mating success in orange-winged males, but had no influence on the mating success of clear-winged males. The orange-winged male flight muscle ratios (FMRs) were significantly higher than the clear-winged male and female FMRs. However, there was no difference in the size-corrected fat reserves of the two morphs; both had higher fat reserves than females. The gain in mass between eclosion and reproduction in orange-winged males and females was almost double the mass gained by clear-winged males, suggesting that clear-winged male development is less costly. An experiment in which pre-reproductive levels of nutrition were manipulated confirmed this.     

Experience-dependent recapture rates and reproductive success in male grey mouse lemurs (Microcebus murinus)

Male mating tactics can vary according to the potential for scramble or contest competition but also as a consequence of individual characteristics, such as body condition and previous experience. The influence of experience, i.e., residency, on male recapture rates and reproductive success was studied in a population of free-living grey mouse lemurs. Long-term capture data from 320 individuals revealed that both sexes had very low recapture probabilities within their first year in the study population, but recapture rates declined less sharply during the following years. Capture results and telemetric analyses on 12 focal males revealed that resident males had larger body mass and larger home ranges than new males. Home range size correlated with the number of accessible females, indicating that resident males had higher probabilities to meet mates than new males. The reproductive success of 132 candidate fathers, representing both resident and new males, was determined by means of molecular genotyping. Paternity determination was successful in 38 cases (success rate: 19%). Sixteen resident males and seventeen new males sired offspring. However, in relation to the number of candidate fathers being present in the mating season, resident males were twice as likely to reproduce successfully as new males. These findings suggest experience-dependent reproductive tactics that most likely correspond to a differential spatial knowledge of resources, mates and potential threats. The results generally agree with the predictions made for a scramble competition regime and demonstrate substantial behavioral plasticity in a nocturnal primate species with a dispersed multi-male/multi-female mating system.     

Costs of reproduction in male lizards, Sceloporus virgatus

Models of life history evolution typically assume a balance between the benefits of current reproductive activity and the costs to future reproductive success or survivorship, but empirical studies often find positive correlations between such components of fitness in undisturbed animal populations. I examined possible survivorship costs of reproduction in free-ranging male lizards, Sceloporus virgatus , and found that males with low levels of mating success were less likely to survive to the following breeding season. I also investigated two possible indicators of reproductive effort, increase in ectoparasite load and decrease in body weight during the breeding season. Levels of parasitism with trombiculid mites at the end of the breeding season were not associated with any measure of fitness or body condition (mating success, survivorship to the following year, relative weight loss). Yearling males (which have low levels of mating success) usually gained weight during the breeding season, while older males generally lost weight during this period. This suggests that young males may have postponed reproduction in favor of body growth and that seasonal weight loss of older males might reflect reproductive effort. Within the group of older males, individuals with the highest levels of mating success did not have high levels of either weight loss or mortality. Mate guarding behavior, an alternative to the aggressive territorial behavior typical of many lizard species, may allow certain males to obtain mates without expending large amounts of energy or exposing themselves to great mortality risks.     

Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris)

In territorial polygynous taxa, reproductive success reflects phenotypic variation. Using Crotaphytus collaris, a sexually dimorphic lizard in which males use the head (i.e., jaws and associated musculature) as a weapon when territorial interactions escalate to fights, we tested the hypothesis that weapon performance (i.e., bite force) is a better predictor of fitness than body or weapon size. Bite-force performance predicted the number of female home ranges overlapped, estimated mating success, and potential reproductive output. However, no body or weapon size measure correlated with these estimates of fitness, and only one weapon dimension (head width) correlated with bite force. These results indicate that weapon performance has far stronger effects on fitness than body or weapon size, likely because it directly influences fight outcomes. As such, it is desirable that the use of morphology as a proxy for performance and its presumed extensions to fitness be based on empirical morphology-performance relationships.     

The effects of social isolation on steroid hormone levels are modulated by previous social status and context in a cichlid fish

Social isolation is a major stressor which impacts the physiology, behaviour and health of individuals in gregarious species. However, depending on conditional and contextual factors, such as social status and group composition, social isolation may be perceived differently by different individuals or even by the same individuals at different times. Here we tested the effects of social status (territorial vs. non-territorial) and previous group composition (i.e. type of social group: mixed sex group with two territorial males, TT vs. mixed sex group with one territorial and one non-territorial male, TnT) on the hormonal response (androgens and cortisol) to social isolation in a cichlid fish (Oreochromis mossambicus). The different steroid hormones measured responded differentially to social isolation, and their response was modulated by social factors. Social isolation elicited a decrease of 11-keto formation only in territorial males, whereas non-territorial males present a non-significant trend for increasing KT levels. Testosterone did not respond to social isolation. Cortisol only increased in isolated individuals from TnT groups irrespective of social status (i.e. both in territorials and non-territorials). These results suggest that it is the perception of social isolation and not the objective structure of the situation that triggers the hormonal response to isolation.