Schistosome monogamy: who,how, and why?

Schistosomes represent a unique animal model for comparative analyses of monogamy. Indeed, schistosomes are classified at the lowest taxonomical level of monogamous species and lack complex social interactions, which could alter our understanding of their unusual mating system. Elements discussed here include the fact that monogamy in schistosomes could be an ancestral state between hermaphroditism and polygyny or polygynandry and the occurrence of mate changes. In addition, hypotheses are proposed to explain monogamy in schistosomes (e.g. female dispersion, the need for paternal care, oviposition site limitation or aggressiveness, and mate guarding). We also propose future experimental and analytical approaches to improve our understanding of the schistosomes' mating system.     

Habitat, Niche, and Evolution of Sirenian Mating Systems

Lek polygyny, monogamy and scramble promiscuity have been reported in the two families and five species of Recent sirenians. Evidence for lek mating in the dugong or "sea pig" (Dugong dugon), monogamy in Steller's sea cow (Hydrodamalis gigas), and scramble promiscuity in the three manatees or "river cows" (Trichechus manatus, Trichechus senegalensis, and Trichechus inunguis), as well as in one dugong population, is reviewed. Sirenians are long-lived "K-strategists" with precocious young, few potential young per female lifetime, high female investment in a few young, little apparent opportunity for post-copulatory male investment, and "paenungulate" reproductive physiologies that appear to increase uncertainty as to female receptivity and assurance as to paternity. Common features notwithstanding, diverse habitats, climates, and niches may account for mating system diversity. Scenarios for evolution of diverse mating systems, based on our understanding of mating systems in terrestrial herbivores, are presented. The dugong retains the ancestral low latitude marine, seagrass dependent, bottom-feeding, niche characteristic of diverse, tusked, Oligocene and Miocene sirenian faunas. With a long breeding season and high polygyny potential, retention of tusks by male dugongs in the absence of any foraging function suggests that tusks may have always had social functions and lekking may be of ancient origin. The sea cow lineage, isolated on the shoreline of the northeastern Pacific as seagrasses declined, turned to surface foraging on chemically undefended kelps and lost both tusks and molar teeth. As it followed kelps northwards, adaptation to a cold-temperate climate compressed the breeding season, limited the polygyny potential, and, in conjunction with incentives for paternal investment, favored pair bonding and the monogamous mating system postulated by George Steller (1751). Manatees, evolving in botanically-rich fresh waters of the Amazon basin as an aberrant offshoot of the marine dugongid line, remained in the tropics and retained a high polygyny potential, but became generalist foragers in the upper few meters of the water column. Labyrinthine river systems provided little opportunity for male aggregation and display (or rhizome foraging) and tusks were lost as the uncertainty of female inseminability drove the mating system toward scramble promiscuity and sperm competition. An observation of manatee-like behavior in a dense and sedentary dugong population in eastern Australia suggests plasticity in sirenian mating, and the likelihood that a form of scramble promiscuity may exist where no suitable site for lekking is available, where large group size makes female defence impossible, or where vulnerability of territorial males to hunting has resulted in extirpation of a lekking tradition. Dugong and manatee life history characteristics conform to expectations based on observed differences in mating systems.     

鸟类婚配制度的生态学分类

在Ｅmlen和Ｏring鸟类婚配制度生态学分类系统的基础上,根据近年来鸟类行为生态学研究的成果,对鸟类的婚配制度进行了补充分类,并强调了应以进化稳定策略的观念来认识乌类的婚配制度。补充的鸟类婚配制度生态型包括：合作型一雄一雌制（cooperative monogamy)、临界型一雄一雌制（critical monogamy)、保卫雌性型一雄一雌制（female defense mognogamy)、从领域型一雄多雌制（poly-terri-tory polygyny)和社群繁殖制。合作型一雄一雌制的鸟 类雌雄个体爱力合作才保证繁殖的成功;临界型一悲欢离合一雌制鸟类雌雄个体都有多配倾向,但迫于生态压力必须共同抚育后代才能繁殖成功;保卫雌性型一雄一雌制的鸟 类通过保卫一个雌鸟不被其它雄鸟占有而保证繁殖成功,多领域型一雄多雌制的雄鸟通过占有多个领域而多个雌鸟交配;社群繁殖制的鸟 类由三个以上个体参与工部分参与繁殖,所有个体共同抚育一批后代,现有的鸟类婚配制度可以归为一雄一雌制（monogamy)、一雄多雌繁殖,所有个体共同抚育一批后代。现有的鸟类婚配制度可以归为一雄一雌制(polygyny)、一雌多雄制（polyandry)快速多窝型多配制（rapid-multiple-clutch polygamy)和社群繁殖制（social breeing systen）五大类型。     

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation

Male androgen responses to social challenges have been predicted to vary with mating system, male-male aggressiveness, and the degree of paternal investment in birds ("challenge hypothesis," Am. Nat. 136 (1990), 829). This study focused on the interspecific predictions of the challenge hypothesis. Comparative methods were used to control for effects of the phylogenetic relatedness among the sampled species. Male androgen data of 84 bird species were collected from literature records on seasonal androgen patterns. From these, the androgen responsiveness (AR) was calculated as described in the original challenge hypothesis (i.e., maximum physiological level/breeding baseline). Scatterplots of AR versus mating strategy, male-male aggressiveness, and the degree of paternal care confirmed the expected interspecific patterns. When phylogenetic analyses were performed among all of the sampled species, the effects of paternal investment disappeared while the AR remained covarying to a high degree with mating system and male-male aggressiveness. Although these mechanisms may be different at the intraspecific level, this suggests that interspecific differences of AR in male birds may have evolved in response to changes of mating strategies, rather than in response to altered paternal duties. However, control for phylogeny among the subsample of 32 passerine species revealed that if any paternal investment contributed to the observed variance in AR, then the change from "no male incubation" to "male shares incubation duties" represented the most effective, whereas the male's contribution to feeding offspring did not explain the observed variation of AR.     

Path analysis and the relative importance of male-female conflict, female choice and male-male competition in water striders

Three major behavioural mechanisms underlying sexual selection in many systems are male-male competition, female choice and male-female conflict. We used path analysis to evaluate the relative importance of these mechanisms in generating sexual selection on a suite of male traits in the stream-dwelling water strider, Aquarius remigis. To gather data for the analysis, we quantified the morphology (total length, limb length, forefemur width, genital length), behaviour (activity), mating frequency, mean mating duration and overall mating success of 96 adult males over a 10-day period. Males varied considerably in mating success. Over the 10 days, individual males mated 0-14 times, spending 0-67% of their time in copula. Path analysis showed that male-male competition was important in favouring larger males with longer limbs that tended to be more active. Active males should encounter females more frequently. In water striders, almost all male-female encounters result in intense premating struggles pitting female resistance to mating against male insistence. This male-female conflict favoured larger males with longer genitalia. These traits help males overcome female resistance. Female choice was expressed via female-controlled variation in mate-guarding durations. Female choice favoured smaller males perhaps because they are lighter, less expensive ‘shields’ against harassment by other males. Male size thus affected mating success via all three behavioural mechanisms. Weak, overall sexual selection favouring larger males was the product of conflicting effects: male-female conflict strongly favouring larger males and male-male competition weakly favouring larger males, offset by female choice favouring smaller males. Separate analyses for warmer versus colder days showed that on colder days (daily high below 20 °C), male-male competition was the main mechanism generating variation in mating frequency, while on warmer days, both male-male competition and male-female conflict were important. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Male Choice and Male-male Competition in Idotea baitica (Crustacea,Isopoda)

Sexual selection in mate-guarding Crustacea may involve several processes: male choice, male-male competition, and female choice. To evaluate the relative importance of the different processes in mate choice of the aquatic isopod I. baitica we studied 1) the mate-choice criteria of males, 2) effects of sex ratio on the outcome of the mating contest, and 3) the role of size in male-male interactions. When given a choice between a small and a large female, males most often chose the one that matured earlier for parturial ecdysis. Maturity was a more important choice criterion than female size, but these also correlated positively. Large males had a mating advantage in both male- and female-biased sex ratios; pairing was size-assortative only in the male-biased ratio where guarding was also longer. If an extra male was placed with a precopulatory pair, 30 % take-overs occurred, large males surpassing. Present and earlier work suggests that male size is an asset in both intra- and intersexual interactions. There is little or no direct phenotypic sexual selection on female size: sexual selection for large males presumably contributes to the evolution of sexual size dimorphism in I. baitica.     

Punishment of polygyny

We investigated the evolution of monogamy (one male, one female) and polygyny (one male, more than one female). In particular, we studied whether it is possible for a mutant polygynous mating strategy to invade a resident population of monogamous breeders and, alternatively, whether a mutant monogamy can invade resident polygyny. Our population obeys discrete-time Ricker dynamics. The role of males and females in the breeding system is incorporated via the harmonic birth function. The results of the invasability analysis are straightforward. Polygyny is an evolutionarily stable strategy mating system; this holds throughout the examined range of numbers of offspring produced per female. So that the two strategies can coexist, polygyny has to be punished. The coexistence of monogamy and polygyny is achieved by reducing the offspring number for polygyny relative to monogamy. This yields long-term persistence of the strategies for all offspring numbers studied. An alternative punishment is to increase the sensitivity of polygynous breeders to population density. The coexistence is possible only with a limited range of offspring produced. The third way to achieve coexistence of the two mating strategies is to assume that individuals live in a spatially structured population, where dispersal links population subunits to a network. Reducing the dispersal rate of polygynous breeders relative to that of monogamous individuals makes the coexistence feasible. However, for monogamy to persist, the number of offspring produced has to be relatively high.     

Faithful without care: the evolution of monogyny

The traditional paradigm of male polygamy and female monogamy has been replaced by the recognition that both sexes may typically mate with several partners. As a consequence, much attention has focused on the evolution of polyandry, while the evolutionary significance of monogyny (male monogamy) remains poorly understood. Monogyny, a taxonomically widespread mating system that includes dramatic examples of male self-sacrifice, is predicted when the benefits of paternal investment exceed those of searching for additional mates. However, monogyny also occurs in animals lacking paternal investment, instead representing a form of paternity protection. It has been suggested that such mating systems are expected where the costs of mate search for males are high. However, this argument fails to recognize that if there is a low probability of a male finding a mate, then there may be a high probability that he will not need to defend his paternity. Using a mathematical model, we show that monogyny as a means of increasing paternity is favored when the sex ratio is male biased, but not necessarily by high search costs. The importance of a male-biased sex ratio for the evolution of monogyny is supported by various empirical studies.     

Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context

Members of a population often differ significantly in theirparental investment. Such variation is generally believed tohave important consequences for mating system evolution andhas been suggested to play an important role in the evolutionof some secondary sexual traits and displays. Recent studiessuggest that individuals are able to adjust the intensity and kindof parental investment they provide according to the breedingconditions they encounter. As a consequence, between-individualvariation in parental investment may depend more on externalconditions than previously thought for these taxa. This mayhave important implications for current perspectives on therole of differential parental investment in the evolution andmaintenance of certain mating systems and sexual selection regimes.Here I quantify patterns of variation in paternal investmentas a function of social conditions in a species of beetle thatis dimorphic for male horn morphology. I demonstrate that undercertain conditions (namely, the absence of other males), paternalassistance covaries with male morphology, with horned males investingsubstantially more time in assisting females than hornless males.I also show that the magnitude of differences in paternal investmentbetween male morphs varies in response to external conditions.In the presence of other males, paternal assistance was negligiblefor both male morphs, who instead invested substantially andequally in mate-securing behaviors. I use my findings to discussthe significance of variation in paternal assistance for onthophaginemating systems and evaluate ideas proposed to explain the evolutionof alternative morphologies in the genus Onthophagus.     

Marriage Systems and Pathogen Stress in Human Societies

Pathogen stress is an important form of environmental extremenessand uncertainty for humans as well as other organisms. It ispredicted to: fl] increase the degree of polygyny (as fewermales become appropriate mates); [2] make non-sororal polygynymore frequent (as variable offspring become more advantageous),and [3] be correlated with signs of sexual selection: physicaldimorphism, societal rules about allowed wives for men in differentcategories, both achieved and inherited. The first two hypotheses are supported. As pathogen stress increases,the degree of polygyny increases, no matter how polygyny ismeasured. As pathogen stress increases, non-sororal polygynyand capture of women from outside societies increase; sororaland other endogamous forms of polygyny decrease. The third hypothesisis not supported. Measures of male-male competition and reflectionsof male status are not associated with pathogen stress. A man'sactual present appearance (physical, behavioral) may providea more direct and accurate reflection of a man's worth as amate. It is possible that the measures available for testinghere are not fully appropriate. These results suggest that major pathogens may have been, duringhuman evolutionary history, an important selective force, shiftingthe polygyny threshold, and resulting in greater polygyny, andpolygyny of specific types, in areas of high stress. The relationshipappears to be of a threshold sort (at high levels of pathogenstress monogamy, polyandry, and mild polygyny are absent) ratherthan a linear relationship. We need within-society data forappropriate pathogens regarding relationship between individualpathogen load and probability of getting a mate, possible interactionsbetween pathogen stress and resource accumulation in sexualselection, and impact of pathogen load on fertility.     

Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged

When male investment in mating varies with quality, reliable sexual signals may evolve. In many songbirds, testosterone mediates mating investment, suggesting that signals should be linked to testosterone production. However, because testosterone may change rapidly during behaviour such as territorial aggression and courtship, efforts to establish such a relationship have proved challenging. In a population of dark-eyed juncos, we measured individual variation in the production of short-term testosterone increases by injecting gonadotropin-releasing hormone (GnRH). We found a positive correlation between the magnitude of these increases and the size of a plumage ornament ('tail white') previously shown to be important for female choice and male-male competition. We then measured naturally elevated testosterone levels produced during male-male competition and found that they covaried with those induced by GnRH. We suggest that the association between tail white and testosterone increases may allow conspecifics to assess potential mates and competitors reliably using tail white.     

Mammalian mating systems

Male mammals show a diverse array of mating bonds, including obligate monogamy, unimale and group polygyny and promiscuity. These are associated with a wide variety of different forms of mate guarding, including the defence of feeding and mating territories, the defence of female groups and the defence of individual receptive females. Female mating bonds include long-term monogamy, serial monogamy, polyandry and promiscuity. Both male and female mating behaviour varies widely within species. Variation in male mating behaviour is related to the effect of male assistance in rearing young and to the defensibility of females by males. The latter is, in turn, related to female ranging behaviour and to the size and stability of female groups. Much of the variation in mammalian mating bonds and systems of mate guarding can be attributed to differences in these three variables.     

Sexual size dimorphism and phylogeny in North American minnows

Sexual size dimorphism (SSD) is predicted to vary across mating systems. A previous study examined a model of SSD in fishes as it relates to three mating system variables: probability of sperm competition, male territorial guarding, and male-male contest. I tested the ability of these variables to predict SSD in North American freshwater minnows, after controlling for phylogenetic effects by an independent contrasts method. Across 58 species only male territorial guarding was significandy related to SSD in a stepwise multiple regression. When tested for 26 genera and subgenera, both male territorial guarding and male-male contest were significant in the model. The concentrated-changes test revealed that character changes in SSD (from males the same size or smaller than females, to males larger than females) were more concentrated on branches with presence of male guarding (similar results were found for changes in SSD and presence of sperm competition), at the species and genus levels. Both comparative approaches demonstrated that male guarding and male-male contest variables are linked to SSD in minnows.     

Sexual dimorphism,mating system,and effect of phylogeny in De Brazza's monkey (Cercopithecus neglectus)

De Brazza's monkey (Cercopithecus neglectus), like other guenons, shows marked sexual dimorphism in an array of features. While strong sexual dimorphism is generally associated with a polygynous mating system, populations of De Brazza's monkeys in Gabon are reportedly monogamous. An explanation of this unique phenomenon is offered here. Patterns of sexual dimorphism are examined for morphology, growth and development, behavior, and ecology, and field and captive studies on the social organization and mating system of De Brazza's monkey and congeneric guenon species are reviewed. Based on the findings, it is postulated that 1) De Brazza's monkeys are not strictly monogamous, but exhibit interpopulational variation in their mating system, from facultative monogamy to mild polygyny; 2) marked sexual dimorphism most likely reflects the effect of the historical-phylogenetic factor; ie, it represents a holdover of a degree of dimorphism established earlier in evolutionary history when the degree of polygyny Was higher; and 3) lessening in the degree of polygyny and a tendency toward monogamy represents a consequence of selection toward small group size. Small group size, a unique antipredator strategy, and failure to form polyspecific associations are ultimately most likely the result of intragroup and interspecific competition and predation pressure.     

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.     

Monogamy as a Rule Rather than Exception in Nocturnal Lemurs: the Case of the Fat-tailed Dwarf Lemur, Cheirogaleus medius

According to present hypotheses on the evolution of life history traits and social systems in Malagasy lemurs, nocturnality and infant parking are associated with a solitary lifestyle and a polygynous mating system. However, theoretically extreme seasonality of reproduction could limit the number of females that can be monopolized by a given male and thus hinder the evolution of polygyny. The aim of this ongoing study is to test these contrasting expectations by looking at the social and mating system of the fat-tailed dwarf lemur Cheirogaleus medius . This species hibernates for up to 7 mo, so that time for breeding and raising offspring is extremely limited.
A mark-recapture study in western Madagascar was combined with observations and radio-tracking of 36 individuals during the rainy seasons from 1995 to 1998. According to these data, fat-tailed dwarf lemurs live in permanent sleeping groups consisting of a male and a female (n = 8) or one male and two females (n = 1). One or two offspring from the previous year were frequently observed to sleep together with an adult pair. Members of each sleeping group were the exclusive users of their nest holes and home ranges. During the birth season, males and females took turns at baby-sitting their offspring. Females without paternal help were unable to raise their offspring successfully. Since females did not exhibit oestrus synchrony, the ultimate selective factor favouring pair-living could be obligate paternal investment. The results, together with the lack of sexual size dimorphism and relatively small testis size, suggest that the fat-tailed dwarf lemur lives in family groups with a monogamous mating system. A review of the mating systems of nocturnal lemurs shows that monogamy appears to be the rule rather the exception.     

Monogamy when there is potential for polygyny: tests of multiple hypotheses in a group-living fish

Monogamy within social groups where there exists a high potentialfor polygyny poses a challenge to our understanding of matingsystem evolution. Specifically, the traditional explanationthat monogamy evolves due to wide female dispersion, affordingmales little opportunity to defend multiple females, cannotapply. Instead, monogamy in groups potentially arises becausefemales compete for breeding resources such as breeding sites,food, and paternal care. We conducted manipulative experimentsto determine whether females compete over limiting resourceswithin groups of the obligate coral-dwelling goby, Paragobiodonxanthosomus (Gobiidae). Breeding females behaved aggressivelytoward individuals of their own sex and evicted subordinatefemales that were large and mature from the group. Experimentalremoval of nest sites caused breeding partners to breed in alternativenest sites, demonstrating that nest site limitation was notthe cause of female competition. Supplemental feeding resultedin an increase in the fecundity of breeding females but no maturationof subordinate females, demonstrating that food-limited femalefecundity was a likely cause of female competition. Finally,supplemental feeding of breeding pairs demonstrated that thedifference in eggs hatched by fed versus unfed males was lessthan the difference in eggs laid by fed versus unfed females,suggesting that paternal care limitation might also drive femalecompetition. These results suggest that competition over foodand possibly paternal care selects for dominant, breeding femalesto suppress the maturation of subordinate females to minimizecompetition. Monogamy in association with group living is thereforelikely to have evolved because female competition prevents malesfrom utilizing the potential for polygyny.     

The Role of Female Behavior in Maintaining Monogamy of a Coral-Reef Filefish

The corallivorous filefish Oxymonacanthus longirostris is a predominantly monogamous species without parental care. Polygyny reduces female fitness because monogamous females benefit from male assistance with feeding–territory defense that secures both a feeding area and time to feed. I studied the strategy of females to prevent polygyny, with the help of field observations and manipulative field experiments. Monogamous females always behaved aggressively towards intruding floater females. When a caged male or female was placed within the territory of a monogamous pair, the resident female was more likely to pay attention to the caged female than to the caged male. Experimentally transplanted floater females succeeded in settling as secondary females in the monogamous territory more frequently when the resident female was caged. These results suggest that monogamous females behave aggressively towards floater females to defend their mating status; such aggressive behavior is successful in preventing polygyny. Furthermore, the removal experiment showed that polygynous (especially secondary) females moved to territories of widowed males located near them more frequently than monogamous females did. This outcome indicates that polygynous females can change their mating status and escape polygyny by moving to another territory if the opportunity occurs. Thus, female behavior can play an important role in the maintenance of monogamy and in lowering the level of polygyny within populations of this species.     

Female sand gobies prefer good fathers over dominant males

Female preference for males successful in male-male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra- and intersexual selection in the sand goby, Pomatoschistus minutus, a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the ''best'' males.