Alternative Reproductive Behaviors Research Articles

Emergence of Alternative Reproductive Tactics in Simulated Robot Colonies

Alternative reproductive behaviour, in which individuals of one sex adopt different ways to reproduce, is observed in all major taxa, including mammals, amphibians, insects, and particularly fishes. In order to study ecological conditions for emergence of alternative reproductive tactics (ARTs), we developed an embodied evolution framework incorporating ecological features, such as body size and energy maintenance, where male and female robotic agents naturally face both intersexual and intrasexual interactions for survival and reproduction. We performed simulation experiments in environments with different conditions (food density, reproductive cost, and male-female ratio) and found that ARTs emerged both in males and females. Males evolved three kinds of alternative tactics: fixed, genetically distinct ARTs, in which dominant and sneaker males that differ in body size adopt different tactics to gain access to females, conditionally flexible ARTs, in which individuals change tactics according to body size, and mixed ARTs, in which combinations of genetically fixed and conditionally flexible ARTs are employed. Females evolved two genetically distinct ARTs: quality-oriented female, QoF, and number-oriented female, NoF, in which females increase fitness either by offspring quality or quantity, respectively. Analysis of results confirms the experimental notions that genetically fixed male ARTs are strongly affected by intensity of sexual selection. Conditionally flexible male ARTs are significantly affected by competition level, and female ARTs are mainly affected by food availability. To our knowledge, this study is the first to demonstrate emergence of ARTs in both males and females from an initially monomorphic population in a simulated, embodied evolution framework.

Hunting regulation favors slow life histories in a large carnivore

As an important extrinsic source of mortality, harvest should select for fast reproduction and accelerated life histories. However, if vulnerability to harvest depends upon female reproductive status, patterns of selectivity could diverge and favor alternative reproductive behaviors. Here, using more than 20 years of detailed data on survival and reproduction in a hunted large carnivore population, we show that protecting females with dependent young, a widespread hunting regulation, provides a survival benefit to females providing longer maternal care. This survival gain compensates for the females’ reduced reproductive output, especially at high hunting pressure, where the fitness benefit of prolonged periods of maternal care outweighs that of shorter maternal care. Our study shows that hunting regulation can indirectly promote slower life histories by modulating the fitness benefit of maternal care tactics. We provide empirical evidence that harvest regulation can induce artificial selection on female life history traits and affect demographic processes.

Seasonal variation in male alternative reproductive tactics.

Genetic parentage analyses reveal considerable diversity in alternative reproductive behaviours (e.g. sneaking) in many taxa. However, little is known about whether these behaviours vary seasonally and between populations. Here, we investigate seasonal variation in male reproductive behaviours in a population of two-spotted gobies (Gobiusculus flavescens) in Norway. Male two-spotted gobies guard nests, attract females and care for fertilized eggs. We collected clutches and nest-guarding males early and late in the breeding season in artificial nests and used microsatellite markers to reconstruct parentage from a subset of offspring from each nest. We hypothesized that mating, reproductive success and sneaking should be more prevalent early in the breeding season when competition for mates among males is predicted to be higher. However, parentage analyses revealed similar values of mating, reproductive success and high frequencies of successful sneaking early (30% of nests) and late (27% of nests) in the season. We also found that multiple females with eggs in the same nest were fertilized by one or more sneaker males, indicating that some males in this population engage in a satellite strategy. We contrast our results to previous work that demonstrates low levels of cuckoldry in a population in Sweden. Our results demonstrate marked stability in both the genetic mating system and male alternative reproductive tactics over the breeding season. However, sneaking rates may vary geographically within a species, likely due to local selection influencing ecological factors encountered at different locations.

De novo sequencing of the Hypericum perforatum L. flower transcriptome to identify potential genes that are related to plant reproduction sensu lato.

BackgroundSt. John’s wort (Hypericum perforatum L.) is a medicinal plant that produces important metabolites with antidepressant and anticancer activities. Recently gained biological information has shown that this species is also an attractive model system for the study of a naturally occurring form of asexual reproduction called apomixis, which allows cloning plants through seeds. In aposporic gametogenesis, one or multiple somatic cells belonging to the ovule nucellus change their fate by dividing mitotically and developing functionally unreduced embryo sacs by mimicking sexual gametogenesis. Although the introduction of apomixis into agronomically important crops could have revolutionary implications for plant breeding, the genetic control of this mechanism of seed formation is still not well understood for most of the model species investigated so far. We used Roche 454 technology to sequence the entire H. perforatum flower transcriptome of whole flower buds and single flower verticils collected from obligately sexual and unrelated highly or facultatively apomictic genotypes, which enabled us to identify RNAs that are likely exclusive to flower organs (i.e., sepals, petals, stamens and carpels) or reproductive strategies (i.e., sexual vs. apomictic).ResultsHere we sequenced and annotated the flower transcriptome of H. perforatum with particular reference to reproductive organs and processes. In particular, in our study we characterized approximately 37,000 transcripts found expressed in male and/or female reproductive organs, including tissues or cells of sexual and apomictic flower buds. Ontological annotation was applied to identify major biological processes and molecular functions involved in flower development and plant reproduction. Starting from this dataset, we were able to recover and annotate a large number of transcripts related to meiosis, gametophyte/gamete formation, and embryogenesis, as well as genes that are exclusively or preferentially expressed in sexual or apomictic libraries. Real-Time RT-qPCR assays on pistils and anthers collected at different developmental stages from accessions showing alternative modes of reproduction were used to identify potential genes that are related to plant reproduction sensu lato in H. perforatum.ConclusionsOur approach of sequencing flowers from two fully obligate sexual genotypes and two unrelated highly apomictic genotypes, in addition to different flower parts dissected from a facultatively apomictic accession, enabled us to analyze the complexity of the flower transcriptome according to its main reproductive organs as well as for alternative reproductive behaviors. Both annotation and expression data provided original results supporting the hypothesis that apomixis in H. perforatum relies upon spatial or temporal mis-expression of genes acting during female sexual reproduction. The present analyses aim to pave the way toward a better understanding of the molecular basis of flower development and plant reproduction, by identifying genes or RNAs that may differentiate or regulate the sexual and apomictic reproductive pathways in H. perforatum.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1439-y) contains supplementary material, which is available to authorized users.

Female preference for sympatric vs. allopatric male throat color morphs in the mesquite lizard (Sceloporus grammicus) species complex.

Color polymorphic sexual signals are often associated with alternative reproductive behaviors within populations, and the number, frequency, or type of morphs present often vary among populations. When these differences lead to assortative mating by population, the study of such polymorphic taxa may shed light on speciation mechanisms. We studied two populations of a lizard with polymorphic throat color, an important sexual signal. Males in one population exhibit orange, yellow, or blue throats; whereas males in the other exhibit orange, yellow, or white throats. We assessed female behavior when choosing between allopatric and sympatric males. We asked whether females discriminated more when the allopatric male was of an unfamiliar morph than when the allopatric male was similar in coloration to the sympatric male. We found that female rejection of allopatric males relative to sympatric males was more pronounced when males in a pair were more different in throat color. Our findings may help illuminate how behavioral responses to color morph differences between populations with polymorphic sexual signals contribute to reproductive isolation.

High Urban Breeding Densities Do Not Disrupt Genetic Monogamy in a Bird Species

Urbanization causes widespread endangerment of biodiversity worldwide. However, some species successfully colonize cities reaching higher densities than in their rural habitats. In these cases, although urban city dwellers may apparently be taking advantage of these new environments, they also face new ecological conditions that may induce behavioural changes. For example, the frequency of alternative reproductive behaviours such as extra-pair paternity and intraspecific brood parasitism might increase with breeding densities. Here, using a panel of 17 microsatellites, we tested whether increments in breeding densities such as those associated with urban invasion processes alter genetic monogamy in the burrowing owl Athene cunicularia. Our results show low rates of extra-pair paternity (1.47%), but relatively high levels of intraspecific brood parasitism (8.82%). However, we were not able to detect differences in the frequency at which either alternative reproductive behaviour occurs along a strong breeding density gradient. Further research is needed to properly ascertain the role of other social and ecological factors in the frequency at which this species presents alternative reproductive strategies. Meanwhile, our results suggest that genetic monogamy is maintained despite the increment in conspecific density associated with a recent urban invasion process.

Adaptive value of same-sex pairing in Laysan albatross

Same-sex pairing is widespread among animals but is difficult to explain in an evolutionary context because it does not result in reproduction, and thus same-sex behaviour often is viewed as maladaptive. Here, we compare survival, fecundity and transition probabilities of female Laysan albatross in different pair types, and we show how female-female pairing could be an adaptive alternative mating strategy, albeit one that resulted in lower fitness than male-female pairing. Females in same-sex pairs produced 80% fewer chicks, had lower survival and skipped breeding more often than those in male-female pairs. Females in same-sex pairs that raised a chick sometimes acquired a male mate in the following year, but females in failed same-sex pairs never did, suggesting that males exert sexual selection by assessing female quality and relegating low-quality females into same-sex pairs. Sexual selection by males in a monomorphic, non-ornamented species is rare and suggests that reconsideration is needed of the circumstances in which alternative reproductive behaviour evolves. Given the lack of males and obligate biparental care in this species, this research demonstrates how same-sex pairing was better than not breeding and highlights how it could be an adaptive strategy under certain demographic conditions.

Reproductive behaviour and the system of signalling inNeurobasis chinensis(Odonata, Calopterygidae) – a kinematic analysis

The reproductive behaviour of the damselfly Neurobasis chinensis (Calopterygidae) was filmed at 300 and 600 frames per second in Thailand in spring 2009. This was subsequently viewed in slow motion for detailed analysis. Altogether we observed 26 matings at two different sites. Besides visual observations of behaviour of male–female encounters at the reproductive sites, we analysed their flight cinematographically by measuring velocity, wing beat frequency, phase relationships of fore- and hind wings, and described the flight paths of different flight manoeuvres. Wing clapping by the perched insects was analysed in detail. Also filmed were alternative reproductive behaviour and avoidance behaviour when attacked by a hunting spider. By analysing the video footage in slow motion, details of male flight with hind wings held motionless, a typical flight-style for this genus, were revealed. The significance of this behaviour in interactions with conspecifics is discussed.

Alternative Mating Strategies in Male Morphotypes of the Prawn Macrobrachiumidellaidella (Hilgendorf, 1898)

An alternative reproductive behaviour can be defined as any discontinuous variation in an aspect of reproductive behaviour among one sex within a single population. Alternative reproductive behaviours occur in a wide variety of taxa and, when referring to particular aspects of the mating behaviour are commonly termed alternative mating tactics. A close examination of M. idellaidella males reveals that three distinct morphotypes based upon size ranking, the ratio of claw length to body length (relative claw length) which included small male (SM), medium size male (MS) and bigger size male (BS). To know the alternative mating strategies 7 experiments were conducted. The following stocking combinations were tried in the present study: (1) 3 BS males (110-120mm) Vs female (55-90mm); (2) 3 MS males (70-80 mm) Vs female (55-90mm); (3) 6 SM males (45-55 mm) Vs female (55-90mm); (4) 1 blocked BS male and 2 MS males Vs female (55-90mm); (5) 1 BS male and 2 MS males Vsfemale (55-90mm); (6) 1 blocked BS male and 5 SM males Vs female (55-90mm); (7) 1 BS male and 5 SM males Vs female (55-90mm) respectively.

Reproductive behavior of the male rose bitterling Rhodeus ocellatus as influenced by the operational sex ratio

Abstract Background Game theory predicts that as the operational sex ratio (OSR; the ratio of sexually active males to fertilizable females) increases, reproductive males may adopt alternative reproductive behaviors. Empirical studies indicated that alternative behaviors may differ for different species. In the present study, we investigated the influence of different male-biased OSRs on male reproductive behaviors shown by a freshwater fish, the rose bitterling Rhodeus ocellatus. Results Six levels of the OSR (1:1, 2:1, 3:1, 5:1, 7:1, and 9:1) were established, and male leading, aggression, and preoviposition ejaculation behaviors were recorded. Our experiments showed that at low OSRs, the leading behavior of male rose bitterling increased with an increasing OSR, reaching a maximum at an OSR of 3:1, and then decreased as the OSR further increased. In contrast, aggression and preoviposition ejaculation behavior continually increased with an increasing OSR. Notably, males possibly lost their territorial position to other males and became sneakers when facing more rivals. Conclusions These observations suggest that at lower OSRs, male rose bitterling mainly rely on leading behavior, while at higher OSRs, they increasingly adopt aggression and preoviposition ejaculation. Therefore, for the rose bitterling, (1) decreased leading behavior and (2) increased aggression and preoviposition ejaculation are two alternative responses in the face of an increasing OSR, which is a more straightforward strategy for facing an increased risk of sperm competition than that adopted by its congener, the European bitterling.

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth-brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth-brooding cichlids is discussed.

Males do not catch up with females in pursuing flight inCalopteryx splendens(Odonata: Calopterygidae)

Abstract In high densities males of Calopteryx splendens showed alternative reproductive behaviour at the river Oker in northern Germany. One of several tactics was to pursue females. Pursuing flight was filmed in summer 2006 in slow motion. Frame by frame analysis showed that males fly in irregular flight patterns: they showed different lengths of wing beat phases in comparison to females which fly more steadily. Females had significantly lower wing beat frequencies than males. The flight patterns of males depended on their position to other pursuing males and to the pursued female. The possible causes of these flight differences are discussed.

Female alternative reproductive behaviors: The effect of female group size on mate assessment and copying

Extensive theoretical and empirical research has focused on male alternative reproductive tactics. In comparison, female alternative tactics have attracted little attention, and further theoretical and empirical research are needed. Using a game theoretical model, we examine female choice alternatives (1) by considering assessment errors in a novel and more realistic manner than done previously, and (2) for the first time, by highlighting the formation of groups of females as an important consequence of copying behavior. We consider two alternatives: direct assessment of male quality by females and female copying of the choice of other females. Assessment and copying are predicted to coexist under a wide variety of circumstances and copying is favored when females make assessment errors, when high-quality males are either common or very rare, and when female fitness declines with the number of other females choosing the same male. We also find that the frequency of copying at equilibrium is predicted to decrease when the presence of other females mating with the same male has a positive effect on female fitness (e.g. through increased male parental effort, decreased predation risk or cooperation among females). Female alternative choice tactics also influence the potential for sexual selection. In our model, when the frequency of copying females is low, the potential for sexual selection can be higher than in the absence of female copying. However, contrary to previous theory, we find that as copying females become more common than assessing females, the potential for sexual selection will be low as more females copy the mate choice of other copiers without assessment.

Male mating tactics in the American rubyspot damselfly: territoriality, nonterritoriality and switching behaviour

Odonates exhibit a wide range of territorial and nonterritorial mating tactics and are ideal for investigating alternative reproductive behaviours. We studied male mating tactics in the American rubyspot damselfly, Hetaerina americana , a species that exhibits red wing spots that have been suggested to have evolved as a consequence of male–male contests. In this species mating success is enhanced by the ability of males to defend territories along streams and rivers, which depends on the amount of thoracic fat reserves available. Previous studies on this species have distinguished between territorial and nonterritorial males, in which the former obtain significantly more matings than the latter. In our study, however, we found a third reproductive tactic: switching. Switcher males exhibit both territorial and nonterritorial tactics and a mating success similar to that of territorial and nonterritorial males, although this result may be confounded by the small sample size used for this analysis. We suggest that the different mating tactics may be condition determined: territorial males contained the highest fat reserves, nonterritorial males had the least fat content and switchers had intermediate fat loads. We also show that there were no age differences between males using these tactics. Our results suggest that territorial behaviour is extremely plastic in this species. Finally, we discuss the implications of our study and directions for future work on territorial and nonterritorial reproductive tactics in odonates.

Threshold dimorphism in ejaculate characteristics in the squid Loligo bleekeri

Male dimorphism has been thought to correlate with alternative reproductive behav- iors. Alternative reproductive behaviors promote asymmetry in sperm competition, and the differ- ences in fertilization success could promote adaptations in ejaculate characteristics in relation to each reproductive behavior. Using allometric analysis, we show that ejaculate dimorphism clearly exists in males of the squid Loligo bleekeri, a cephalopod species with body size-related alternative mating behaviors. A morphological switch point was detected for internal characters: larger individuals pro- duced discontinuously longer spermatophores than did smaller individuals, although no switch point was detected for external characteristics (fin length, fin width, head width, mantle width, tentacle length and hectocotylus length) except for bimodal body size. This clear internal switch point could be an adaptation to the characteristic alternative mating behaviors of loliginid squid, in which males use different mating tactics to pass spermatophores to different sperm storage sites in and on the females. Our results indicated that alternative reproductive behaviors can result in morphological adjustment in internal characteristics.

Operational Sex Ratio and Alternative Reproductive Behaviours in Chinese Bushcricket, Gampsocleis gratiosa

AbstractThe effects of operational sex ratio (OSR) on male mating tactics in the Chinese bushcricket Gampsocleis gratiosa were investigated in male‐ and female‐biased environments. We measured fresh and dry spermatophore contents and copulation duration, and counted sperm numbers of each copulation. The fresh weight of spermatophore and spermatophylax was positively correlated with male body weight. The males in a strongly male‐biased environment produced significantly heavier fresh ampulla and more sperm per ejaculation, which were likely tactics for successful matings under the competition of rivals. The spermatophore might function as a structure to protect the fertilization potential of the ejaculate from rival males.

Dependance of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri

The mating behavior of captive Loligo bleekeri and the paternity of the resulting prog- eny were examined based on behavioral observations and genetic analyses. In this species, there are 3 mating behaviors (male-parallel, head-to-head, and extra-pair), and 2 sperm storage sites in females (seminal receptacle and the opening of the oviduct), which suggest that sperm competition occurs. All 3 mating behaviors were observed, and females mated often with different males, result- ing in multiple paternity within 3 of the 4 broods examined. In each brood, the male to mate last and frequently before the female spawned fertilized the most eggs (87 to 100%). A sneaker male that mated by extra-pair copulation sired 8.5% of the eggs in a brood. Some eggs were fertilized by sperm received before the start of the study, indicating that sperm can be stored for at least several days before a spawning. In the broods with multiple paternity, the paternity patterns differed among egg capsules. Male competition was more intense between similar-sized males than between different- sized males, but body size did not affect the copulative success in the male-parallel position. We found multiple mating and multiple paternity in L. bleekeri. Paternity rates differed depending on the complex of factors, mating position, timing, frequency and duration. Alternative reproductive be- haviors would change these factors and lead to different paternity rates.

Genetic mating system and timing of extra-pair fertilizations in the Kentish plover

It is still unclear why females in many bird species pursue extra-pair copulations. Current hypotheses focus mainly on indirect benefits such as obtaining particular “good genes” for their offspring or maximizing genetic compatibility between themselves and the father of their offspring. Supporting the latter, a recent study of shorebirds suggests that extra-pair matings may function to avoid the negative effects of genetic similarity between mates. Here, we further investigate genetic parentage in the Kentish plover, Charadrius alexandrinus, a shorebird with a highly variable social mating system. DNA fingerprinting revealed that most pairs were genetically monogamous: 7.9% of the broods (7/89) contained extra-pair young, comprising 3.9% of all chicks (9/229). These cases represented, however, three alternative reproductive behaviors: extra-pair paternity, quasi-parasitism (extra-pair maternity) and intraspecific brood parasitism. This is the first study showing the occurrence of all three behaviors in one shorebird species. We also found that extra-pair fertilizations (extra-pair paternity and quasi-parasitism) were more frequent later in the breeding season. There was no consistent relationship between genetic similarity of mates and laying date; the pattern, as well as the degree of genetic similarity, differed among breeding sites within the study population.

Male morphological variation and the determinants of body size in two Otiteselline fig wasps

The chalcid wasps (Hymenoptera) that develop in fig tree inflorescences (Ficus: Moraceae) have often been used to study alternative reproductive behaviors. However, recent work suggests that such behaviors are more complex than previously thought. We investigated this in Otitesella longicauda and O. rotunda. In addition to known dimorphisms in the two species (each have ‘‘religiosa’’ males that use their mandibles to fight for mates in the fig, and ‘‘digitata’’ males that disperse from the fig to mate), we found that religiosa males below species-specific body size switch points have relatively larger mandibles and are less sclerotized than those above. Thus, they are actually trimorphic. We suggest that the religiosa morph variation is linked to fighter/nonfighter alternative mating behaviors, with small (nonfighting) males having relatively larger mandibles because they also use them to pull females out of their galls before mating. Also, we investigated the determinants of wasp body size, and whether females (foundresses) adjust their offspring allocation strategies according to expected offspring size. We found that wasp size is larger in ovaries near the center of the fig, and more females and fewer religiosa males are laid in such ovaries than in those further away. This probably indicates that foundresses lay females when they are expected to be large because their fitness is more body size‐dependent than that of religiosa males. We then discuss the implications of our findings for the study of alternative reproductive behaviors and foundress offspring allocation strategies. Key words: alternative reproductive behaviors, body size‐dependent fitness effects, fig wasps, offspring allocation strategies. [Behav Ecol 15:735–741 (2004)]

Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus

We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.