Monogamous Mating System Research Articles

The Social System of Lariang Tarsiers (Tarsius lariang) as Revealed by Genetic Analyses

Previous sociobiological studies of tarsiers were invariably based on field observations. Sulawesi tarsiers are known for monogamous or facultative polygynous social mating systems, but, to date, no data exist to describe the genetic mating system. We here bring together behavioral studies and molecular tools for the first time to elucidate mating behavior and kinship within a tarsier population. We investigated the social system of the recently described Tarsius lariang, which researchers have never studied before. Between September and November 2005, we conducted field observations and sampling in central Sulawesi, Indonesia, where this species is endemic. Ten of 11 social groups of the focal population were composed of 1 adult male, 1 adult female, and putative offspring. To enlighten genetic relationships, we used 12 microsatellite loci and mitochondrial DNA sequences of 26 captured and sampled Lariang tarsiers for parentage and relatedness analyses. A significant number of young were the offspring of the sampled group adults, suggesting a predominantly monogamous social and genetic mating system. There is evidence for extrapair young in groups in which adult pairs exhibit close relationships, leading to the assumption that extrapair mating is solicited to avoid inbreeding. Ten of 11 social groups lived in monogamous social systems, indicating monogamy to be the rule in Tarsius lariang.

Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca

Extrapair paternity may create marked variation in the reproductive success of males and thus contribute to the evolution of sexually selected traits in socially monogamous mating systems. We examined the distribution of extrapair paternity in a passerine bird, the pied flycatcher, in relation to plumage coloration and male age. The frequency of extrapair paternity was found to be low in our study population in Southwest Finland (38 of 857 (4.4%) offspring in 25 of 191 (13%) broods). We were able to identify the sire for 53% of the extrapair young and in each case the extrapair sire was at least 2 years old. The probability of siring extrapair young was not associated with pigment-based brown-black dorsal plumage coloration, structural ultraviolet (UV) coloration or forehead patch size. The probability of being cuckolded, however, increased with decreasing UV chroma of the white wing patch. Our results thus indicate that there are multiple factors influencing when and with whom females engage in extrapair copulations. They also indicate that the male traits influencing the decision to cuckold the social mate are different from those used for choosing an extrapair mate.

Why some rails have white tails: the evolution of white undertail plumage and anti-predator signaling

Conspicuous plumage patches have evolved in birds as conspecific signals for mate attraction and assessment, intersexual competition or to signal alarm. Signals may alternatively be directed at potential predators to discourage pursuit. Rails (Family Rallidae) are ground-dwelling birds, many of which inhabit wetlands, while others occur in forests and grasslands. They are renown for their secretive nature and the tendency to flick their tails when observed. This behavior is more conspicuous in species with white undertail coverts that contrast sharply with darker body plumage. Using species comparisons and controlling for phylogeny, we investigated four hypotheses for the evolution of white undertail coverts in rails. We found little support for the hypothesis that white tails are sexually selected: white tails were not more common in species with polygamous as opposed to monogamous mating systems, species with sexual dimorphism, nor species that display their tails in courtship. Nor did our results support the hypothesis that white tail plumage evolved for intersexual competition during territorial interactions. Instead, we found that species that flock for at least part of the year and species found in open as opposed to concealing habitats were significantly more likely to have white undertail coverts. Rail species inhabiting concealing habitats are less commonly gregarious and more likely selected for crypsis. Using phylogenetically-controlled statistical inference we found that adaptation to open wetland habitats significantly precedes the evolution of white undertails, whereas gregariousness likely evolved later in some lineages. The inferred order of trait evolution suggests that this plumage characteristic could have been selected primarily for enhancement of an anti-predator signal rather than a social signal for conspecifics.

Group formation and anemone use in captively reared anemonefish (Amphiprion frenatus)

We studied group formation and anemone use in captively reared anemonefish Amphiprion frenatus. Four small fish (23–32 mm total length) were simultaneously released into a central area of the aquaria (ca. 160 l) that was divided in half with an anemone placed on each half, with the opportunity to settle on either side. Four-day trials were conducted for analyzing settlement patterns. Because of the monogamous mating system, we predicted that small fish should settle in pairs. However, all four small fish settled on the same side in 7 of 14 replicates, which was a higher than expected value under random settlement.

Socio-genetic structure of mound-building mice, Mus spicilegus, in autumn and early spring

Mus spicilegus has become a popular biological model species in the last decade because of the evolutionary interest of its behavioural particularities (the building of mounds, bi-parental care and monogamous mating system). The genetic structure of M. spicilegus populations should reflect those life-history traits. Although many studies have reported on mound-building mouse populations in the field or in a semi-natural enclosure, only one used hyper variable genetic markers to assess parentage and social structure. In the present study conducted in Hungary, we analysed individuals from seven highly populous mounds in autumn with the set of loci used in a previous study. Our results confirmed that mounds are inhabited by juveniles from several parental units, but revealed population differences. In a capture–recapture field session in spring, we assessed genetic relationships between individuals after dispersal from the mounds, the other key moment of the life cycle of this species. The results indicate that the social structure at this moment reflects a transition phase between the large over-wintering groups and the monogamous pairs described later in the year. Social bounds forged during the long winter cohabitation may have lasting effects on social and genetic structure of this species. This scenario is discussed in respect of the available literature on this species as well as other species.

Seasonal variation in male-female competition, cooperation and selfish hoarding in a monogamous songbird

Both cooperation and conflict between the sexes are commonplace in monogamous mating systems. However, little is known about how cooperation and competition varies seasonally in monogamous species that maintain permanent territories. We presented territorial pairs of male and female New Zealand robins (Petroica australis) with a large supply of insect prey at monthly intervals for 2 years. Behavioural observations after food presentation were then made to quantify seasonal and sexual differences in aggressive interactions over prey, prey acquisition rates, mate provisioning, offspring provisioning, selfish food hoarding and cache retrieval. Data were used to evaluate sex-specific behavioural strategies of mediating competition for food. Results showed that males aggressively excluded females from experimental food sources year-round. Females only accessed food sources when males left them unattended. Consequently, females acquired fewer prey than males. After controlling for differences in prey acquisition, both sexes consumed similar amounts of prey in the non-breeding season. Even though males aggressively excluded females from accessing food sources directly, males fed large amounts of prey to females during the breeding season. Both sexes provisioned young at similar rates. Males cached less prey than females in the breeding season but more prey than females in the non-breeding season. Females showed similar caching intensities year-round. Although males tried to defend their hoards, females frequently retrieved male-made caches. Overall, results showed that although New Zealand robins cooperate to raise offspring during the breeding season, conflict between the sexes occurs year-round. Males and females display different behavioural strategies to gain access to experimental food sources, which appear to lessen male–female competition for food and evenly distribute food resources between the sexes.

A comparison of social behaviour in two rodent species: implications for the mating system of mound‐building mice, Mus spicilegus

Mound‐building mice, Mus spicilegus, and house mice, Mus musculus musculus, are closely related species, sympatric in northern Bulgaria. Many studies report a polygynous mating system in populations of M. m. musculus, but little is known about the mating system of M. spicilegus. Mus spicilegus displays some behavioural features of social monogamy, but the presence of monogamy has been questioned. To test whether M. spicilegus is monogamous, patterns of amicable and agonistic behaviour in M. spicilegus and M. m. musculus were studied in intraspecific male–male, female–female and male–female dyadic encounters. Results indicated that M. spicilegus displayed significantly less amicable, more defensive and more offensive behavioural events than M. m. musculus. The higher aggressiveness of M. spicilegus seems to be more compatible with a monogamous mating system than with a polygynous one.

OFF-TERRITORY FORAYS AND GENETIC MATING SYSTEM OF THE WOOD THRUSH (HYLOCICHLA MUSTELINA)

Abstract Extrapair fertilizations (EPFs) are an important component of many socially monogamous mating systems. However, information about the reproductive tactics used by male and female birds in extrapair mating systems is still rare. We used radiotelemetry to measure territory use, forays, and mate association in Wood Thrush (Hylocichla mustelina) when females were fertile and not fertile. We also conducted paternity analysis to determine the frequency of EPFs in our study population. Socially paired male and female Wood Thrush maintained a close physical association while on their own territory. Most of the off-territory forays observed during the fertile stage were conducted by social pairs. Lone males rarely engaged in off-territory forays during their mate's fertile period but made relatively frequent off-territory forays when their mates were not fertile. Male Wood Thrush may trade-off investment into paternity assurance and extrapair tactics by favoring a mate-guarding tactic when their within-pa...

Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlanica, off the Pacific coast of Panama

A previous study predicted the evolution of monogamy in symbiotic crustaceans inhabiting scarce, relatively small hosts in tropical environments where predation risk away from hosts is high. This prediction was tested in the shrimp Pontonia margarita, which inhabits the pearl oyster Pinctada mazatlanica. A total of 68 oysters were collected from the intertidal and shallow subtidal at two islands (Islas Secas [N 27° 55′, W 82° 03′] and Isla de La Coiba [N 27° 50′, W 97° 03′]) off the eastern tropical Pacific coast on 15 and 17 March 2007, respectively. The population structure, distribution, male-female association pattern, and relative growth of the major claw and pleura of the second abdominal segment of each shrimp retrieved were examined. Shrimps were found as heterosexual pairs in the mantle cavity of hosts more frequently than would be expected by chance alone. Males occurred with females in the same host, independent of the reproductive condition of the female or the stage of development of brooded embryos. This observation, and strong correlations between the host and shrimp body size in both males and females suggest a long-term association between males and females in each host. Sexual dimorphism in body size was minor, with males being just slightly smaller than females. In agreement with predictions for monogamous species, the major claw of males did not display positive allometry, which has been generally reported for polygamous shrimps. In turn, the pleura of the second abdomen presented negative allometry in males but positive allometry in females. All available information suggests that Pontonia margarita has a socially monogamous mating system with males and females forming exclusive pairs in their hosts.

The population dynamical implications of male-biased parasitism in different mating systems.

Although there is growing evidence that males tend to suffer higher levels of parasitism than females, the implications of this for the population dynamics of the host population are not yet understood. Here we build on an established ‘two-sex’ model and investigate how increased susceptibility to infection in males affects the dynamics, under different mating systems. We investigate the effect of pathogenic disease at different case mortalities, under both monogamous and polygynous mating systems. If the case mortality is low, then male-biased parasitism appears similar to unbiased parasitism in terms of its effect on the population dynamics. At higher case mortalities, we identified significant differences between male-biased and unbiased parasitism. A host population may therefore be differentially affected by male-biased and unbiased parasitism. The dynamical outcome is likely to depend on a complex interaction between the host's mating system and demography, and the parasite virulence.

Histological description of seminiferous epithelium and cycle length of spermatogenesis in the water shrew Neomys fodiens (Mammalia: Soricidae)

Recently, we examined the spermatogenesis cycle length in two shrews species, Sorex araneus characterized by a very high metabolic rate and a polyandric mating system (sperm competition) resulting in a short cycle and Crocidura russula characterized by a much lower metabolic rate and a monogamous mating system showing a longer cycle. In this study, we investigated the spermatogenesis cycle in Neomys fodiens showing an intermediate metabolic rate. We described the stages of seminiferous epithelium according to the spermatid morphology method and we calculated the cycle length of spermatogenesis using incorporation of 5-bromodeoxyuridine into DNA of the germ cells. Twelve males were injected intraperitoneally with 5-bromodeoxyuridine, and the testes were collected. For cycle length determination, we applied a recently developed statistical method. The calculated cycle length is 8.69 days and the total duration of spermatogenesis based on 4.5 cycles is approximately 39.1 days, intermediate between the duration of spermatogenesis of S. araneus (37.6 days) and C. russula (54.5 days) and therefore congruent with both the metabolic rate hypothesis and the sperm competition hypothesis. Relative testes size of 1.4% of body mass indicates a promiscuous mating system.

Evolution of mating systems in coral reef gobies and constraints on mating system plasticity

Social and mating systems can be influenced by the distribution, abundance, and economic defendability of breeding partners and essential resources. Polygyny is predicted where males can economically defend multiple females or essential resources used by females. In contrast, monogamy is predicted where neither sex can monopolise multiple partners, either directly or through resource control, but where one mate is economically defendable. The mating system and reproductive behaviour of five species of coral reef goby were investigated and contrasted with population density and individual mobility. The two most abundant species (Asterropteryx semipunctatus and Istigobius goldmanni) were polygynous. In contrast, the less populous and more widely dispersed epibenthic species (Amblygobius bynoensis, Amblygobius phalaena and Valenciennea muralis) were pair forming and monogamous. All five species had low mobility, mostly remaining within metres (3 epibenthic species) or centimetres (2 cryptobenthic species) of a permanent shelter site. Interspecific differences in the mating system may have been shaped by differences in population density and the ability of reproductive individuals to economically defend breeding partners/sites. However, in a test of mating system plasticity, males of the three monogamous species did not mate polygynously when given the opportunity to do so in experimental manipulations of density and sex ratio. Mate guarding and complex spawning characteristics, which have likely co-evolved with the monogamous mating system, could contribute to mating system inflexibility by making polygynous mating unprofitable for individuals of the pair forming species, even when presented with current-day ecological conditions that usually favour polygyny.

Cycle Length of Spermatogenesis in Shrews (Mammalia: Soricidae) with High and Low Metabolic Rates and Different Mating Systems1

The aim of the present study was to establish and compare the durations of the seminiferous epithelium cycles of the common shrew Sorex araneus, which is characterized by a high metabolic rate and multiple paternity, and the greater white-toothed shrew Crocidura russula, which is characterized by a low metabolic rate and a monogamous mating system. Twelve S. araneus males and fifteen C. russula males were injected intraperitoneally with 5-bromodeoxyuridine, and the testes were collected. For cycle length determinations, we applied the classical method of estimation and linear regression as a new method. With regard to variance, and even with a relatively small sample size, the new method seems to be more precise. In addition, the regression method allows the inference of information for every animal tested, enabling comparisons of different factors with cycle lengths. Our results show that not only increased testis size leads to increased sperm production, but it also reduces the duration of spermatogenesis. The calculated cycle lengths were 8.35 days for S. araneus and 12.12 days for C. russula. The data obtained in the present study provide the basis for future investigations into the effects of metabolic rate and mating systems on the speed of spermatogenesis.

Sexual Selection and the Evolution of Brain Size in Primates

Reproductive competition among males has long been considered a powerful force in the evolution of primates. The evolution of brain size and complexity in the Order Primates has been widely regarded as the hallmark of primate evolutionary history. Despite their importance to our understanding of primate evolution, the relationship between sexual selection and the evolutionary development of brain size is not well studied. The present research examines the evolutionary relationship between brain size and two components of primate sexual selection, sperm competition and male competition for mates. Results indicate that there is not a significant relationship between relative brain size and sperm competition as measured by relative testis size in primates, suggesting sperm competition has not played an important role in the evolution of brain size in the primate order. There is, however, a significant negative evolutionary relationship between relative brain size and the level of male competition for mates. The present study shows that the largest relative brain sizes among primate species are associated with monogamous mating systems, suggesting primate monogamy may require greater social acuity and abilities of deception.

Sexually selected females in the monogamous Western Australian seahorse

Studies of sexual selection in monogamous species have hitherto focused on sexual selection among males. Here, we provide empirical documentation that sexual selection can also act strongly on females in a natural population with a monogamous mating system. In our field-based genetic study of the monogamous Western Australian seahorse, Hippocampus subelongatus, sexual selection differentials and gradients show that females are under stronger sexual selection than males: mated females are larger than unmated ones, whereas mated and unmated males do not differ in size. In addition, the opportunity for sexual selection (variance in mating success divided by its mean squared) for females is almost three times that for males. These results, which seem to be generated by a combination of a male preference for larger females and a female-biased adult sex ratio, indicate that substantial sexual selection on females is a potentially important but under-appreciated evolutionary phenomenon in monogamous species.

Harvesting of males delays female breeding in a socially monogamous mammal; the beaver.

Human exploitation may skew adult sex ratios in vertebrate populations to the extent that males become limiting for normal reproduction. In polygynous ungulates, females delay breeding in heavily harvested populations, but effects are often fairly small. We would expect a stronger effect of male harvesting in species with a monogamous mating system, but no such study has been performed. We analysed the effect of harvesting males on the timing of reproduction in the obligate monogamous beaver (Castor fiber). We found a negative impact of harvesting of adult males on the timing of parturition in female beavers. The proportion of normal breeders sank from over 80%, when no males had been shot in the territories of pregnant females, to under 20%, when three males had been shot. Harvesting of males in monogamous mammals can apparently affect their normal reproductive cycle.

Exclusive core areas in overlapping ranges of the sleepy lizard, Tiliqua rugosa

Where animal home ranges overlap extensively, objectively identifying exclusive areas within individual ranges has been difficult, particularly in species lacking overt territorial behaviors. By analyzing the overlap between successively smaller core areas among individuals in a population of the long-lived Australian skink, the sleepy lizard (Tiliqua rugosa), we objectively determined exclusive areas within animal ranges. Using 4-year radio tracking data, we found that ranges consisted of relatively large sally zones (mean 66--80% total range), around home ranges with multinucleate cores strongly associated with key refuge sites. Total range and home range area varied significantly among years, being smaller in a drought year. Total ranges overlapped extensively between and within sexes, but for both sexes, intrasexual overlap of inner range cores rapidly approached zero, suggesting intrasexual territoriality. Intersexual inner core overlap reflected this species socially monogamous mating system. But, male overlap of female ranges and inner cores was consistently higher than female-male overlap. Refuges and/or mates may be defended resources within these core areas, although aggressive behavioral interactions were rarely observed. In the extensively overlapping sally zones, males shared space with females other than their principal partner. In productive years, with larger home ranges and more extensive overlap, some lizards associated with extra partners, suggesting that males opportunistically use sally zones for polygyny. Consequently, we suggest that benefits to females from male association may change with environmental quality, such that if food resources are low, monogamy may be favored if females increase foraging efficiency as a consequence of male vigilance during pairing. Copyright 2006.

Testosterone in Females: Mediator of Adaptive Traits, Constraint on Sexual Dimorphism, or Both?

When selection on males and females differs, the sexes may diverge in phenotype. Hormones serve as a proximate regulator of sex differences by mediating sex-biased trait expression. To integrate these perspectives, we consider how suites of traits mediated by the same hormone in both sexes might respond to selection. In male birds, plasma testosterone (T) varies seasonally and among species according to mating system. When elevated experimentally, it is known to enhance some components of fitness and to decrease others. We report that female T also varies seasonally and co-varies with male T. Female T is higher in relation to male T in sexually monomorphic species and is higher absolutely in females of species with socially monogamous mating systems, which suggests adaptation. We also consider the effect of experimentally elevated T on females and whether traits are sensitive to altered T. We hypothesize that sensitive traits could become subject to selection after a natural change in T and that traits with opposing fitness consequences in males and females could constrain dimorphism. Results from birds, including the dark-eyed junco (Junco hyemalis), reveal many sensitive traits, some of which appear costly and may help to account for observed levels of sexual dimorphism.

Sexual Selection and the Evolution of Visually Conspicuous Sexually Dimorphic Traits in Male Monkeys, Apes, and Human Beings

Striking secondary sexual traits, such as brightly colored "sexual skin," capes of hair, beards, and other facial adornments occur in adult males of many anthropoid primate species. This review focuses upon the role of sexual selection in the evolution of these traits. A quantitative approach is used to measure sexually dimorphic characters and to compare their development in the monogamous, polygynous, and multimale-multifemale mating systems of monkeys, apes, and human beings.

Sexual selection, redundancy and survival of the most beautiful.

A model is described of a highly redundant complex organism that has overlapping banks of genes such that each vital function is specified by several different genetic systems. This generates a synergistic profile linking probability of survival to the number of deleterious mutations in the genome. Computer models show that there is a dynamic interaction between the mean number of new deleterious mutations per generation (X), the mean number of deleterious mutations in the genome of the population (Y) and percentage zygote survival (Zs). Increased X leads to increased Y and a fall in Zs but it takes several generations before a new equilibrium is reached. If sexual attraction is influenced by the number of deleterious mutations in the genome of individuals then Y is reduced and Zs increased for any given value of X. This fall in Y and rise in Zs is more marked in polygamous than monogamous mating systems. The model is specified such that deleterious mutations can occur without any observable or measurable effect on function. Thus sexual selection, in this organism, for low levels of deleterious mutations cannot be based on assessment of performance. Instead it is based on a simple symmetrical surface pattern that is flawlessly reproduced by organisms with no deleterious mutations, but is less than perfect, and therefore less attractive, if genetic systems have been deleted. A complex vital task requires a system with a high level of redundancy that acts so that the loss of one component has no observable effect and therefore cannot be used for sexual selection. The reproduction of a beautiful surface pattern also requires a low error, high redundancy genetic system; however, in this case there is advantage if a single deleterious mutation produces a recognisable change. This leads to the conclusion that sexual selection and sexual attraction should be based on beauty rather than utility, and explains the common observation in nature that it is the most beautiful that survive.