The Social System of Lariang Tarsiers <Emphasis Type="Italic">(Tarsius lariang)</Emphasis> 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.     

Genetic and Social Monogamy – Does It Occur Without Mate Guarding in the Ringed Plover?

Among birds, waders (suborder Charadrii) show a remarkable variation in social mating systems. Their genetic mating systems are, however, less well known, especially in socially monogamous species. Here, we use DNA fingerprinting and behavioral studies to examine genetic parentage and male mate guarding in the ringed plover Charadrius hiaticula , a monogamous wader with biparental care. None of the putative parents was excluded as a genetic parent of the chicks attended (57 young from 21 families). Statistical resampling supported that extra-pair parentage occurs only rarely, if ever, in the ringed plover. We found no evidence for male mate guarding by close following as a paternity assurance strategy. Lack of extra-pair paternity in the ringed plover is therefore probably not a consequence of male mate guarding, but of high costs and/or low benefits from extra-pair copulations for females.     

Social structure and facultative mating systems of hoary marmots (Marmota caligata)

Mate-choice theory predicts different optimal mating systems depending on resource availability and habitat stability. Regions with limited resources are thought to promote monogamy. We tested predictions of monogamy in a social rodent, the hoary marmot (Marmota caligata), at the northern climatic extreme of its distribution. Mating systems, social structure and genetic relationships were investigated within and among neighbouring colonies of marmots within a 4 km(2) valley near Kluane National Park, Yukon, Canada, using 21 microsatellite loci. While both monogamous and polygynous populations of hoary marmots have been observed in the southern reaches of this species' range; northern populations of this species are thought to be predominantly monogamous. Contrary to previous studies, we did not find northern hoary marmot social groups to be predominantly monogamous; rather, the mating system seemed to be facultative, varying between monogamy and polygyny within, as well as among, social groups. These findings reveal that the mating systems within colonies of this species are more flexible than previously thought, potentially reflecting local variation in resource availability.     

Strict monogamy in a semi-colonial passerine: the Jackdaw Corvus monedula

In this study we used DNA fingerprinting to provide an accurate measure of paternity in a nest-box colony of Jackdaws. The species is a semi-colonial, socially monogamous passerine which establishes long-term pair bonds. Parents raise a single annual brood in which 50% brood reduction is commonplace. However, nest sites are a limited resource, non-breeding adults are also common around colonies and males are frequently separated from their incubating females during the fertile egg-laying period so that opportunities arise for extra-pair copulation. The parentage analysis, however, revealed no cases of extra-pair fertilisation (EPF) or intra-specific brood parasitism. Therefore fledgling output or survival is likely to be a good measure of individual reproductive success in this species. The lack of EPFs is not explained by nesting synchrony and we discuss the relative costs and benefits to females of seeking EPFs; the likelihood that paternal care and a life-history strategy similar to many long-lived non-passerines may also constrain the species to monogamy.     

Adaptation to monogamy influences parental care but not mating behavior in the burying beetle,Nicrophorus vespilloides

The mating system is expected to have an important influence on the evolution of mating and parenting behaviors. Although many studies have used experimental evolution to examine how mating behaviors evolve under different mating systems, this approach has seldom been used to study the evolution of parental care. We used experimental evolution to test whether adaptation to different mating systems involves changes in mating and parenting behaviors in populations of the burying beetle, Nicrophorus vespilloides. We maintained populations under monogamy or promiscuity for six generations. This manipulation had an immediate impact on reproductive performance and adult survival. Compared to monogamy, promiscuity reduced brood size and adult (particularly male) survival during breeding. After six generations of experimental evolution, there was no divergence between monogamous and promiscuous populations in mating behaviors. Parents from the promiscuous populations (especially males) displayed less care than parents from the monogamous populations. Our results are consistent with the hypothesis that male care will increase with the certainty of paternity. However, it appears that this change is not associated with a concurrent change in mating behaviors.     

Using probability modelling and genetic parentage assignment to test the role of local mate availability in mating system variation

The formal testing of mating system theories with empirical data is important for evaluating the relative importance of different processes in shaping mating systems in wild populations. Here, we present a generally applicable probability modelling framework to test the role of local mate availability in determining a population's level of genetic monogamy. We provide a significance test for detecting departures in observed mating patterns from model expectations based on mate availability alone, allowing the presence and direction of behavioural effects to be inferred. The assessment of mate availability can be flexible and in this study it was based on population density, sex ratio and spatial arrangement. This approach provides a useful tool for (1) isolating the effect of mate availability in variable mating systems and (2) in combination with genetic parentage analyses, gaining insights into the nature of mating behaviours in elusive species. To illustrate this modelling approach, we have applied it to investigate the variable mating system of the mountain brushtail possum (Trichosurus cunninghami) and compared the model expectations with the outcomes of genetic parentage analysis over an 18-year study. The observed level of monogamy was higher than predicted under the model. Thus, behavioural traits, such as mate guarding or selective mate choice, may increase the population level of monogamy. We show that combining genetic parentage data with probability modelling can facilitate an improved understanding of the complex interactions between behavioural adaptations and demographic dynamics in driving mating system variation.     

Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus

Seahorses (Hippocampus spp.) are non-sex-role-reversed members of the Syngnathidae family that provide extensive brood care. Previous studies of seahorses have revealed monogamy within a single brood, but their longer term mating system had not been comprehensively evaluated. The parental contribution to 29 wild-born broods of Hippocampus guttulatus, sampled from six Portuguese populations with differing seahorse densities and sex ratios, was assessed using microsatellite DNA markers. To assess the longer term genetic mating system of this species parentage was determined in eleven broods sampled from a captive population over two breeding seasons. Genetic data suggest that this socially polygamous seahorse is serially monogamous across breeding seasons, i.e. monogamous within a season but may switch mates between seasons, and that differing population densities and sex ratios do not affect the mating system.     

田鼠属动物婚配制度的研究范式

从社会组织的生态格局、熟悉性、社会等级和交配近况等择偶行为的影响因子,性二型和雄性射精能力等个体特征,配对关系的神经内分泌机制几方面综述了田鼠动物婚配制度的研究进展,同时从生态学、比较心理学、生理学、神经生物学等方面探讨择偶行类节式的特点。生态学方法,用鼠动物具有完整的婚配制度多样性格局,是婚配制度比较研究的哺乳动物类群。运用比较心理学方法,通过择偶行为实验可直接比较单配制与较研究的理想哺乳动物类     

High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii

The Australian lizard Egernia stokesii lives in spatially and temporally stable groups of up to 17 individuals. We have recently shown that these groups are comprised of breeding partners, their offspring and, in some cases, highly related adults, providing the first genetic evidence of a family structure in any lizard species. Here we investigated the mating system of E. stokesii using data from up to eight polymorphic microsatellite loci and tested the hypothesis that breeding partners are monogamous both within and between mating seasons. Among 16 laboratory-born litters from field collected gravid females from two sites in South Australia, 75% had a single male parent and no male contributed to more than one litter, indicating a high level of genetic monogamy within a season. Additional analyses of field caught individuals, captured between 1994 and 1998, enabled assignment of parentage for 70 juveniles and subadults. These data showed that most young (88.6%) had both parents from within the same group and that high proportions of males (88.9%) and females (63.6%) have multiple cohorts of offspring only with the same partner. Our results suggest that monogamy both within and between seasons is a common mating strategy of E. stokesii and that breeding partners maintain stable associations together and with multiple cohorts of their offspring over periods of up to at least 5 years.     

Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

High frequency of extrapair copulation with low level of extrapair fertilization in the Lanyu scops owl Otus elegans botelensis

The genetic mating system is known for only a few species of owls. Most of them are genetically monogamous. The Lanyu scops owl Otus elegans botelensis breeds in high density in the forests of Lanyu (Orchid Island), southeast of Taiwan. Because extra-pair copulations (EPCs) have frequently been observed, we suspected a high degree of extra-pair fertilizations (EPFs). Through intensive field observations we quantified both within-pair and extra-pair copulations of this owl, and used a set of microsatellite loci to assign the parentage of 200 offspring from 108 families collected between 1999 and 2004. Among copulations for which we could identify both participants, 19.77% were EPC. However, no EPC was observed in the period just before egg laying. We found only two cases of parentage mismatch among 108 broods. The first case was most likely a case of brood usurpation, which would be the first case reported in the Strigidae. The second case was an EPF resulting in one offspring. Our study found that parentage mismatch in the Lanyu scops owls to be extremely low, therefore reproductive success can be estimated accurately by simply counting chicks in nests.     

Monogamy in marine fishes

The formation of long-term pair bonds in marine fish has elicited much empirical study. However, the evolutionary mechanisms involved remain contested and previous theoretical frameworks developed to explain monogamy in birds and mammals are not applicable to many cases of monogamy in marine fish. In this review, we summarise all reported occurrences of social monogamy in marine fish, which has so far been observed in 18 fish families. We test quantitatively the role of ecological and behavioural traits previously suggested to be important for the evolution of monogamy and show that monogamous species occur primarily in the tropics and are associated with coral reef environments in which territory defence and site attachment is facilitated. However, there is little evidence that obligately monogamous species are smaller in body size than species that can adopt a polygynous mating system. We review the evidence pertaining to six hypotheses suggested for the evolution of monogamous pair bonds: (1) biparental care, (2) habitat limitation, (3) low population density/low mate availability/low mobility, (4) increased reproductive efficiency, (5) territory defence, and (6) net benefit of single mate sequestration. We outline predictions and associated empirical tests that can distinguish between these hypotheses, and assess how generally each hypothesis explains monogamy within and between breeding periods for species with different types of territories (i.e. feeding only or feeding and breeding). Hypotheses (1) and (2) have limited applicability to marine fishes, while hypotheses (3)-(5) have little empirical support beyond the species for which they were designed. However, the role of paternal care in promoting monogamous pair bonds is not explicit in these hypotheses, yet paternal care has been reported in more than 70 monogamous marine fish. We show that paternal care may act to increase the likelihood of monogamy in combination with each of the proposed hypotheses through decreased benefits to males from searching for additional mates or increased advantages to females from sequestering a single high-quality mate. Among species defending breeding and feeding territories, the benefits, both within and between reproductive periods, of sequestering a single high-quality mate (hypothesis 6) appear to be the best explanation for socially monogamous pairs. For species without parental care (i.e. holding only feeding territories), territory defence (hypothesis 5) in combination with the benefits of guarding a large mate (hypothesis 6) could potentially explain most instances of monogamy. Empirical studies of marine fishes over the past two decades are therefore slowly changing the view of monogamy from a mating system imposed upon species by environmental constraints to one with direct benefits to both sexes.     

The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes

Genomic levels of variation can help reveal the selective and demographic forces that have affected a species during its history. The relative amount of genetic diversity observed on the sex chromosomes as compared to the autosomes is predicted to differ among monogamous and polygynous species. Many species show departures from the expectation for monogamy, but it can be difficult to conclude that this pattern results from variation in mating system because forces other than sexual selection can act upon sex chromosome genetic diversity. As a critical test of the role of mating system, we compared levels of genetic diversity on the Z chromosome and autosomes of phylogenetically independent pairs of shorebirds that differed in their mating systems. We found general support for sexual selection shaping sex chromosome diversity because most polygynous species showed relatively reduced genetic variation on their Z chromosomes as compared to monogamous species. Differences in levels of genetic diversity between the sex chromosomes and autosomes may therefore contribute to understanding the long-term history of sexual selection experienced by a species.     

High frequency of extrapair copulation with low level of extrapair fertilization in the Lanyu scops owl Otus elegans botelensis

The genetic mating system is known for only a few species of owls. Most of them are genetically monogamous. The Lanyu scops owl Otus elegans botelensis breeds in high density in the forests of Lanyu (Orchid Island), southeast of Taiwan. Because extra‐pair copulations (EPCs) have frequently been observed, we suspected a high degree of extra‐pair fertilizations (EPFs). Through intensive field observations we quantified both within‐pair and extra‐pair copulations of this owl, and used a set of microsatellite loci to assign the parentage of 200 offspring from 108 families collected between 1999 and 2004. Among copulations for which we could identify both participants, 19.77% were EPC. However, no EPC was observed in the period just before egg laying. We found only two cases of parentage mismatch among 108 broods. The first case was most likely a case of brood usurpation, which would be the first case reported in the Strigidae. The second case was an EPF resulting in one offspring. Our study found that parentage mismatch in the Lanyu scops owls to be extremely low, therefore reproductive success can be estimated accurately by simply counting chicks in nests.     

Parentage analysis in Gabonese colonies of soil-feeding termites belonging to the Cubitermes sp. affinis subarquatus complex of species (Termitidae: Termitinae)

Abstract Cubitermes spp. are widely distributed soil-feeding termite species in sub-Saharan Africa which play a fundamental role in soil structure and fertility. A complex of at least four cryptic species (i.e., Cubitermes sp. affinis subarquatus complex of species) has been recently described using molecular markers. In order to investigate the breeding system of these species, five microsatellite markers were used to carry out parentage and relatedness analyses in 15 Gabonese colonies. Monogamy was confirmed as the predominant reproductive organization in Cubitermes spp. (76% of the colonies). Within 30% of these monogamous colonies, a high relatedness between reproductives was shown, suggesting that mating between related individuals occurs. However, Cubitermes colonies can deviate from monogamy. Indeed, parental contributions by at least two related reproductives of the same sex were revealed in four colonies and polyandry was demonstrated in two of them. Infiltration of reproductives in the colony is the most plausible explanation for such cases of polygamy in Cubitermes spp.     

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara''s owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.     

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.     

Mating system and timing of breeding in Holarctic waders

In passerine birds polygamous species lay eggs later than monogamous species. Yom-Tov has hypothesized that this is because polygamous males do not provision their mates with food, thereby delaying egg-laying. An indirect prediction of this hypothesis is that there should be no difference in laving dates between monogamous and polygamous birds in which mate provisioning does not occur. This prediction was tested by examining egg-laying dates in sympatric wader species that have contrasting mating systems but in which food provisioning of mates does not occur. Polygamous waders laid eggs later than monogamous waders, however, both in a comparison involving only calidridine sandpipers and in a comparison involving sandpipers and plovers. Accounting for phylogeny did not affect the direction of the results, which therefore cast doubt on the validity of the 'mate provisioning' hypothesis and indicated that features common to both passerines and waders were more likely to explain the differences in egg-laying dates between mating systems. Mating system and parental care system were strongly related, with all polygamous species being uniparental and monogamous species being biparental. It is suggested that seasonally early food supplies are of relatively low abundance, constraining species to biparental care and monogamy. By contrast, seasonally late food supplies are more abundant, making uniparental care more successful, thereby creating greater opportunities for mate desertion and polygamy.