Species cohesion despite extreme inbreeding in a social spider

Colonial social spiders experience extreme inbreeding and highly restricted gene flow between colonies; processes that question the genetic cohesion of geographically separated populations and which could imply multiple origins from predecessors with limited gene flow. We analysed species cohesion and the potential for long-distance dispersal in the social spider Stegodyphus dumicola by studying colony structure in eastern South Africa and the cohesion between this population and Namibian populations previously published. Data from both areas were (re)analysed for historic demographic parameters. Eastern South African S. dumicola were closely related to an east Namibian lineage, showing cohesion of S. dumicola relative to its sister species. Colony structure was similar in both areas with mostly monomorphic colonies, but haplotype diversity was much reduced in eastern South Africa. Here, the population structure indicated recent population expansion. By contrast, Namibia constitutes an old population, possibly the geographic origin of the species. Both the comparison of the eastern South African and Namibian lineages and the distribution within eastern South Africa show the potential for long-distance dispersal in few generations via colony propagation.     

Sexual competition in an inbreeding social spider,Stegodyphus dumicola (Araneae: Eresidae)

Summary Sexual competition is shown to occur in the social spiderStegodyphus dumicola (Eresidae). While the secondary sex ratio inS. dumicola was female-biased, the overall operational sex ratio (numbers of breeding males to breeding females over the season) showed no strong female bias. Males matured before females and had a shorter lifespan than the females. Mating took place in the natal colony. Males fought over access to the few mature females available early in the reproductive season, but females appeared to control the duration of mating. Later in the season, some adults of both sexes dispersed alone to breed elsewhere. We conclude that different rates of maturation between the sexes within a colony provide the opportunity for females that mature early in the season to be choosy in selecting a mate and this forces males to compete. Early reproduction may be beneficial for both females and males, because the offspring of females that reproduce early may have a competitive advantage over later (and smaller) offspring in the colony.     

Spontaneous male death and monogyny in the dark fishing spider

Monogyny (male monogamy) is found in a diverse assemblage of taxa, and recent theoretical work reveals that a male-biased sex ratio can favour the evolution of this relatively rare mating system. We integrate this theoretical framework with field observations and laboratory experiments involving the sexually size dimorphic fishing spider, Dolomedes tenebrosus, to test the prediction that this species exhibits monogyny. Field surveys revealed a male-biased sex ratio, likely resulting from different life-history strategies (early male maturation). Results from mating trials supported our prediction of monogyny as we discovered that males mate with a single female. Unexpectedly, however, we observed that mating results in obligate male death and genital mutilation. Additional field observations of released individuals suggest that males are not limited by their ability to encounter additional females. Controlled laboratory assays demonstrated that males discriminate among virgin and non-virgin female silk cues, consistent with predictions of first-male sperm precedence. In summary, we report a novel case of male self-sacrifice in a species that exhibits female-biased sexual size dimorphism, male-biased sex ratio, genital mutilation and a suggestion of first-male sperm precedence; all of which are consistent with theoretical predictions of the evolution of monogyny.     

Patterns of variation in female-biased colony sex ratios in a social spider

Colonies of a social spider Achaearanea wau (Theridiidae) from Papua, New Guinea have adult and juvenile sex ratios that are biased towards females, and this probably represents a primary bias at the egg stage. Adult sex ratios are less female-biased than are juvenile sex ratios, and both vary significantly among colonies. Adult sex ratios covary with colony size: small colonies have a larger proportion of males than large ones. The pattern of variation in adult sex ratio may be due to greater mortality of females than of males during maturation. Juvenile sex ratios do not covary with colony size, nor do they differ among populations. Colony size, however, does have a significant effect on survival and dispersal in colonies. I conclude, therefore, that a conditional sex ratio strategy, in which the primary sex ratio of the colony is adjusted to changing demographic patterns, does not occur in A. wau. I suggest that environmental heterogeneity acting on individual reproductive output may be responsible for the observed variation among colonies in juvenile sex ratios.     

Strong inbreeding depression in male mating behaviour in a poeciliid fish

The magnitude of inbreeding depression is often larger in traits closely related to fitness, such as survival and fecundity, compared to morphological traits. Reproductive behaviour is also closely associated with fitness, and therefore expected to show strong inbreeding depression. Despite this, little is known about how reproductive behaviour is affected by inbreeding. Here we show that one generation of full‐sib mating results in a decrease in male reproductive performance in the least killifish (Heterandria formosa). Inbred males performed less gonopodial thrusts and thrust attempts than outbred males (δ = 0.38). We show that this behaviour is closely linked with fitness as gonopodial performance correlates with paternity success. Other traits that show inbreeding depression are offspring viability (δ = 0.06) and maturation time of males (δ = 0.19) and females (δ = 0.14). Outbred matings produced a female biased sex ratio whereas inbred matings produced an even sex ratio.     

Microsatellite DNA analysis reveals low diploid male production in a communal bee with inbreeding

The mechanism of sex determination assumed widespread in parthenogenetically arrhen-otokous Hymenoptera is that of single locus complementary sex determination (CSD). Functionally sterile diploid males are produced under CSD and generate a genetic load, the cost of which increases with inbreeding. We quantify diploid male production (DMP, proportion of diploid individuals that are male) using a morphological criterion (adult fresh weight) and genetical (microsatellite DNA) markers in a communal, sexually size-dimorphic bee, Andrma scotica , which inbreeds. Male genotypes suggested a DMP of 0.003. The inbreeding coefficient, f , was significandy positive (+ 0.165), equivalent to 44% of matings being among full sibs (predicted DMP of 0.11). We hypothesize three non-mutually exclusive explanations to account for the large difference between the low observed (in males) and high expected (derived fromy f for females) DMP: (i) multilocus CSD, (ii) 'sex allele signalling' tied to mate selection, and (iii) sperm selection within mated females. The costs of inbreeding through DMP are apparendy low in A. scotica .     

Mate and territory availability affect breeding dispersal and divorce in a resident Southern House Wren Troglodytes aedon musculus population

Breeding dispersal is the movement of an individual between breeding attempts and is usually associated with the disruption of the social pair bond, although mates may disperse together as a social unit. In monogamous territorial species, the decision to disperse may be affected by individual attributes such as sex, age and condition of the disperser. However, environmental and social contexts may also play a crucial role in the decision to disperse. We analysed capture‐resighting data collected over 9 years to study breeding dispersal and divorce rates of a Southern House Wren Troglodytes aedon musculus population in South Temperate Argentina. Between‐season dispersal was more frequent than within‐season dispersal, with females dispersing more often than males, both between and within seasons. Both within‐season and between‐season breeding dispersal probability was affected by territory availability, but not by previous breeding success. When the adult sex ratio (ASR) was more skewed towards males, male between‐season dispersal was also affected by mating status, with widowed and single males dispersing more often than paired males. Within‐season divorce increased the reproductive success of females but not males, and was affected by the availability of social partners (with increasingly male‐skewed ASR). Our results suggest that territorial vacancies and mating opportunities affect dispersal and divorce rates in resident Southern House Wrens, highlighting the importance of social and environmental contexts for dispersal behaviour and the stability of social pair bonds.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Flow cytometric sexing of spider sperm reveals an equal sperm production ratio in a female-biased species

Producing equal amounts of male and female offspring has long been considered an evolutionarily stable strategy. Nevertheless, exceptions to this general rule (i.e. male and female biases) are documented in many taxa, making sex allocation an important domain in current evolutionary biology research. Pinpointing the underlying mechanism of sex ratio bias is challenging owing to the multitude of potential sex ratio-biasing factors. In the dwarf spider, Oedothorax gibbosus, infection with the bacterial endosymbiont Wolbachia results in a female bias. However, pedigree analysis reveals that other factors influence sex ratio variation. In this paper, we investigate whether this additional variation can be explained by the unequal production of male- and female-determining sperm cells during sperm production. Using flow cytometry, we show that males produce equal amounts of male- and female-determining sperm cells; thus bias in sperm production does not contribute to the sex ratio bias observed in this species. This demonstrates that other factors such as parental genes suppressing endosymbiont effects and cryptic female choice might play a role in sex allocation in this species.     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

Role of breeding and natal movements in lifetime dispersal of a forest‐dwelling rodent

The lifetime movements of an individual determine the gene flow and invasion potential of the species. However, sex dependence of dispersal and selective pressures driving dispersal have gained much more attention than dispersal at different life and age stages. Natal dispersal is more common than dispersal between breeding attempts, but breeding dispersal may be promoted by resource availability and competition. Here, we utilize mark–recapture data on the nest‐box population of Siberian flying squirrels to analyze lifetime dispersal patterns. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refer to the nest site changes between breeding attempts. The movement distances observed here were comparable to distances reported earlier from radio‐telemetry studies. Breeding movements did not contribute to lifetime dispersal distance and were not related to variation in food abundance or habitat patch size. Breeding movements of males were negatively, albeit not strongly, related to male population size. In females, breeding movement activity was low and was not related to previous breeding success or to competition between females for territories. Natal philopatry was linked to apparent death of a mother; that is, we did not find evidence for mothers bequeathing territories for offspring, like observed in some other rodent species. Our results give an example of a species in which breeding movements are not driven by environmental variability or nest site quality. Different evolutionary forces often operate in natal and breeding movements, and our study supports the view that juveniles are responsible for redistributing individuals within and between populations. This emphasizes the importance of knowledge on natal dispersal, if we want to understand consequences of movement ecology of the species at the population level.     

Natal dispersal patterns are not associated with inbreeding avoidance in the Seychelles warbler

In this study, we test whether patterns of territory inheritance, social mate choice and female-biased natal dispersal act as inbreeding avoidance mechanisms in the cooperatively breeding Seychelles warbler. Our results show that Seychelles warblers do not reduce the likelihood of inbreeding by avoiding related individuals as mates. The occurrence of natural and experimentally induced territory inheritance did not depend on whether the remaining breeder was a parent of the potential inheritor or an unrelated breeder. Furthermore, dispersing individuals were no less related to their eventual mates than expected given the pool of candidates they could mate with. The female bias in natal dispersal distance observed in the Seychelles warbler does not facilitate inbreeding avoidance because, contrary to our prediction, there was no sex difference in the clustering of related opposite sex breeders around the natal territories of dispersers. As a result, the chance of females mating with relatives was not reduced by their greater dispersal distance compared with that of males.     

Brain carnitine deficiency causes nonsyndromic autism with an extreme male bias: A hypothesis

Could 10–20% of autism be prevented? We hypothesize that nonsyndromic or “essential” autism involves extreme male bias in infants who are genetically normal, but they develop deficiency of carnitine and perhaps other nutrients in the brain causing autism that may be amenable to early reversal and prevention. That brain carnitine deficiency might cause autism is suggested by reports of severe carnitine deficiency in autism and by evidence that TMLHE deficiency ? a defect in carnitine biosynthesis ? is a risk factor for autism. A gene on the X chromosome (SLC6A14 ) likely escapes random X‐inactivation (a mixed epigenetic and genetic regulation) and could limit carnitine transport across the blood‐brain barrier in boys compared to girls. A mixed, common gene variant‐environment hypothesis is proposed with diet, minor illnesses, microbiome, and drugs as possible risk modifiers. The hypothesis can be tested using animal models and by a trial of carnitine supplementation in siblings of probands. Perhaps the lack of any Recommended Dietary Allowance for carnitine in infants should be reviewed. Also see the video abstract here: https://youtu.be/BuRH_jSjX5Y

     

A comparison of techniques for assessing dispersal behaviour in gundis: revealing dispersal patterns in the absence of observed dispersal behaviour

Knowledge of the dispersal status of group members is important to understanding how sociality may have evolved within a species. I assessed the effectiveness of four techniques for elucidating dispersal behaviour in a rock-dwelling rodent ( Ctenodactylus gundi ) with small group sizes (2–10 animals): genetic parentage assignment, haplotype data and kinship analyses, assignment testing, and F -statistics. The first two methods provided the greatest insight into gundi dispersal behaviour. Assignment testing and F -statistics proved of limited use for elucidating fine-scale dispersal, but could detect large-scale patterns despite low sex-biased dispersal intensity (1.9 : 1) because of moderate genetic differentiation among groups ( F _ST = 0.10). Findings are discussed in light of current dispersal theory. In general, gundi dispersal is plastic, and seems to be dependent on body weight (for males), group composition, and scale of analysis (total dispersal events recorded within the population were almost twice the immigration rate into the population). Most groups were comprised of a single matriline and one immigrant male. Immigrant rather than philopatric males bred with group females. Dispersal among groups was male-biased, but dispersal or philopatry could occur by either sex. During a drought, both sexes delayed dispersal and cooperative social units formed. Whether such behaviour resulted directly from the drought or not remains unclear, however, since comparative information was not available from nondrought years. Combining fine-scale analyses with information on large-scale patterns provided substantial insight into gundi dispersal behaviour despite the limited movement of animals during a drought, and may prove useful for elucidating dispersal behaviour in other social animals.     

Reproductive limits and heterogeneity of male twospotted spider mites

This paper determines reproductive limits and variation in performance of male twospotted spider mites Tetranychus urticae Koch when virgin females are provided ad libitum over the first eight days of adult life. Theree phases of male reproduction were studied: copulations, insemination and reproduction. An average one day old male copulated 15 times, inseminated 15 females, and contributed to 336 daughters. All parameters declined with age. The average male inseminated 70 females and contributed to 1145 daughters in the first days. Variability between males was small for all parameters considered. These data suggest that the number of sperm transferred at each insemination, rather than the number of inseminations, is the limiting step to higher male reproductive output.

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Résumé La reproduction est un processus qui nécessite généralement un mâle et une femelle. Cependant la biologie des populations ne s'est traditionnellement intéressée qu'à la contribution des femelles dans ce processus. Un effet de cet accent sur les femelles est que l'activité reproductrice des mâles a été très ignorée. Cet article examine, dans un contexte démographique, l'activité reproductrice des mâles de T. urticae, acarien arrhénotoque et phytophage. Trois séquences de l'activité reproductrice des mâles ont été examinées: 1) la copulation, 2) l'insémination, 3) la reproduction.En moyenne un mâle de 1 jour a copulé 15 fois, inséminé 15 femelles et a eu 336 filles. Pendant les 8 premiers jours, le mâle moyen a inséminé 70 femelles et a eu 1145 filles. Ces résultats suggèrent que le nombre de spermatozoïdes transférés à chaque insémination, plus que le nombre d'inséminations, est le facteur limitant d'une forte contribution du mâle à la reproduction.

     

Body size and social dominance influence breeding dispersal in male Pachydiplax longipennis (Odonata)

1. Dispersal behaviour can be affected by an individual's phenotype, by the environmental or social context they experience, and by interactions between these factors. Differential dispersal propensities between individuals may also be an important modifier of functional connectivity between populations. To assess how a key trait, body size, affected both social interactions and dispersal behaviour, this study examined the relationship between body size, antagonistic interactions, and breeding dispersal in male dragonflies (Pachydiplax longipennis) across a seasonal decline in adult body size. 2. During a seasonal peak in male body size in this study, dispersers were smaller than non‐dispersers. Later in the season, the body size of dispersers and non‐dispersers did not differ. 3. Focal observations found that body size was related to competitive dominance, large males engaged in aggressive chases more often and smaller males were more frequently pursued. 4. These results indicate that when large males were present, small males were more likely to disperse suggesting that dispersal is a tactic adopted by social subordinates in this context. If breeding dispersal is typically undertaken by subordinate males, functional connectivity between populations may be less than estimated from absolute dispersal rates.     

The evolution of social inbreeding mating systems in spiders: limited male mating dispersal and lack of pre‐copulatory inbreeding avoidance in a subsocial predecessor

Cooperation and group living are extremely rare in spiders and only few species are known to be permanently social. Inbreeding is a key characteristic of social spiders, resulting in high degrees of within‐colony relatedness that may foster kin‐selected benefits of cooperation. Accordingly, philopatry and regular inbreeding are suggested to play a major role in the repeated independent origins of sociality in spiders. We conducted field observations and laboratory experiments to investigate the mating system of the subsocial spider Stegodyphus tentoriicola. The species is suggested to resemble the ‘missing link’ in the transition from subsociality to permanent sociality in Stegodyphus spiders because its social period is prolonged in comparison to other subsocial species. Individuals in our two study populations were spatially clustered around maternal nests, indicating that clusters consist of family groups as found in the subsocial congener Stegodyphus lineatus. Male mating dispersal was limited and we found no obvious pre‐copulatory inbreeding avoidance, suggesting a high likelihood of mating with close kin. Rates of polygamy were low, a pattern ensuring high relatedness within broods. In combination with ecological constraints, such as high costs of dispersal, our findings are consistent with the hypothesis that the extended social period in S. tentoriicola is accompanied with adaptations that facilitate the transition towards permanent sociality. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 851–859.     

Phylogeography of lethal male fighting in a social spider mite

When males fight for access to females, such conflict rarely escalates into lethal fight because the risks and costs involved, that is, severe injury or death, are too high. The social spider mite, Stigmaeopsis miscanthi, does exhibit lethal male fights, and this male–male aggressiveness varies among populations. To understand the evolution of lethal fighting, we investigated aggressiveness in 42 populations and phylogenetic relationships in 47 populations along the Japanese archipelago. By analysis of the male weapon morph, a proxy for aggressiveness, we confirmed the existence of a mildly aggressive (ML) form, besides the low aggression (LW) and high aggression (HG) forms reported earlier. To evaluate demographic history of these three forms, we employed the approximate Bayesian computation approach using mtCOI sequences and taking into consideration the postlast glacial expansion history of the host plant, Miscanthus sinensis. As results, hierarchical split models are more likely to explain the observed genetic pattern than admixture models, and the ML form in the subtropical region was considered the ancestral group. The inferred demographic history was consistent with the one reconstructed for the host plant in a previous study. The LW form was split from the ML form during the last glacial period (20,000–40,000 years BP), and subsequently, the HG form was split from the ML form at the end of or after the last glacial period (5,494–10,988 years BP). The results also suggest that the mite invaded Japan more than once, resulting in the present parapatric distribution of LW and HG forms in eastern Japan.