Sociality in the phylogenetically basal allodapine bee genus Macrogalea (Apidae: Xylocopinae): implications for social evolution in the tribe Allodapini

Recent phylogenetic studies based on DNA sequence data indicate that the tropical African bee genus Macrogalea is the sister group to the remaining extant allodapine fauna, whereas previously it was thought to be a distal group. This leads to some fundamental changes in our understanding of social evolution in the allodapines. Earlier studies suggested that Macrogalea showed only weak forms of social behaviour and these were not well characterized. However, large samples of Macrogalea zanzibarica presented here show that this species exhibits marked social behaviour. Nearly half of nests collected contained two or more adult females, with up to 10 females per nest. Brood are reared progressively and brood ages within colonies are staggered, giving rise to colonies with very mixed age structures and therefore frequent opportunities for alloparental care. Ovarian dissections indicate non‐simple forms of reproductive partitioning within colonies and most multi‐female colonies show evidence that more than one female has contributed to egg production, though reproductive episodes among colony members are frequently asynchronous. Some females show signs of much higher wing wear than their nestmates, but always show signs of previous reproduction. Reproductive division of labour appears to be temporally marked, ovarian differentiation among nestmates is linked to relative body size, but permanent worker‐like or queen‐like castes appear to be absent. This is similar to the communal, continuously brooded and multivoltine behaviour of some tropical halictine species and may be due to the aseasonal nature of brood development in tropical regions. Patterns of per capita brood production indicate large benefits to multi‐female nest occupancy, and sex allocation is strongly female biased. These findings strongly suggest that the capacity for complex social interactions and alloparental care is an ancestral trait for all of the extant allodapine lineages. Therefore comparisons among extant allodapines are unlikely to throw light on the initial origin of social behaviour, though they may uncover origins of true caste behaviour and reversals to solitary nesting. Sex ratios in Macrogalea and most other allodapine genera, spanning a broad phylogenetic and ecological range, suggest that one or more allodapine traits have provided persistent selection for female‐biased sex allocation.     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

Reproductive hierarchies in the African allodapine bee Allodapula dichroa (Apidae: Xylocopinae) and ancestral forms of sociality

The social organization of allodapine bees has been described in detail for most genera, although there remains a notable gap for one major lineage, the genus Allodapula . Here, we provide the first detailed study of social organization in Allodapula dichroa . Colony sizes are small and the frequency of cooperative nesting is low compared with other allodapine taxa, but there is very clear evidence for reproductive differentiation among adult nestmates. Reproductively dominant females tend to be larger than their nestmates and have much higher levels of wing wear, suggesting that they perform most foraging activities. Multi-female colonies have: (1) lower rates of complete brood absence, suggesting a substantial benefit to cooperative nesting; and (2) larger numbers of brood, suggesting that the presence of a second adult female leads to a greater reproductive output. These data suggest a major phylogenetic split in the form of social organization within the allodapines. In the genus Macrogalea (sister clade to all other allodapines), body size does not preclude young females from laying eggs, and there appears to be, at most, weak reproductive queues. However, in most other allodapines, reproductive hierarchies are prominent and younger and/or smaller females queue for reproductive opportunities, adopt permanently subordinate roles, or disperse. Interestingly, the most common forms of reproductive hierarchies in allodapines do not involve subordinates undertaking foraging roles before reproduction, but instead involve the delaying of both reproduction and foraging. This has implications for the understanding of suggested developmental ground plans in the early stages of social evolution.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 520–530.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Social and maternal factors affecting duckling survival in eiders Somateria mollissima

1. With the aid of a novel survivorship model, an 8-year field study of social and maternal factors affecting duckling survival in eiders (Somateria mollissima) revealed that duckling survival probability varies in accordance with maternal brood-rearing strategy. This variability in survival provides compelling evidence of different annual fitness consequences between females that share brood-rearing and those that tend their broods alone. Consequently, as prebreeding survival is often a major source of individual variation in lifetime reproductive success, a female's annual, state-dependent (e.g. condition) choice of a brood-rearing strategy can be a critical fitness decision. 2. Variance in duckling survival among lone tender broods was best explained by a model with significant interannual variability in survival, and survivorship tending to increase with increasing clutch size at hatch. Clutch size was correlated positively with female condition. Hatch date and female body condition together affected duckling survival, but their contributions are confounded. We were unable to identify a relationship between female age or experience and duckling survival. 3. Variance in duckling survival among multifemale brood-rearing coalitions was best explained by a model that included the number of tenders, the number of ducklings and interannual variation in how their ratio affected survivorship. Hatch date did not significantly influence survival. 4. Expected duckling survival is higher in early life for lone tenders when compared with multifemale brood-rearing coalitions. However, as ducklings approach 2-3 weeks of age, two or three females was the optimal number of tenders to maximize daily duckling survival. The survivorship advantage of multifemale brood-rearing coalitions was most evident in years of average survival. 5. The observed frequency distribution of female group sizes corresponds with the distribution of offspring survival probabilities for these groups. Evidence for optimal group sizes in nature is rare, but the most likely candidates may be groups of unrelated animals where entry is controlled by the group members, such as for female eiders. 6. Our study demonstrates that differences in social factors can lead to different predictions of lifetime reproductive success in species with shared parental care of self-feeding young.     

Life cycle and social behavior in a heathland population of the allodapine bee,Exoneura bicolor (Hymenoptera: Apidae)

Summary Previous studies of the allodapine beeExoneura bicolor have utilised a predominantly social population from tall montane forests. In this report we examine aspects of the sociality and biology of a population from subcoastal heathland in western Victoria, Australia. Entire colonies, nesting inXanthorrhoea minor, were collected at monthly intervals over 12 months between February 1989 and January 1990. In addition, three collections fromMelaleuca squarrosa were made over three consecutive winter months. The heathland population differs from the montane population in several aspects associated with sociality: (i) it shows lower levels of co-occupancy in both newly founded and re-used nests; (ii) foundress dispersal occurs over a larger proportion of the year; and (iii) there may be a partical second brood produced in late summer, during and after adult eclosion of the first brood. The occurrence of a partial second brood gives rise to opportunities for sib-rearing and eusociality. Colony sizes tend to be larger inM. squarrosa thanX. minor, but still smaller than colonies from the montane population. Egg-laying commences several weeks earlier in multifemale colonies than in single female colonies, before spring dispersal begins. It appears that multifemale colonies are more successful at preventing brood loss than single females and that the mean number of brood per female is larger in multifemale colonies than in single female colonies. These two populations, which display differences in several life history traits, provide an ideal system for studying the mechanisms maintaining social behavior.     

A cost of maternal care in the dung beetle Onthophagus taurus?

Parental care theory assumes that investment in current offspring will trade against future investment. A number of field studies on birds have used clutch size manipulations to demonstrate a survival cost to chick rearing. However, such studies do not account for costs accrued during earlier stages of reproduction because not all aspects of reproductive effort are manipulated by varying the number of nestlings. In this study, we investigate the effect of reproductive effort on female survival in the dung beetle, Onthophagus taurus. By experimentally manipulating mating status and dung availability, we demonstrate that virgin females survive longer than mated females and that the survival of mated females was negatively associated with the number of brood masses produced. Using a novel manipulation of the mating system, we separated the effects of egg production and maternal care on female survival. Previously, we have shown that females provisioning with the assistance of a major male provide relatively less care than unassisted females. However, paternal assistance did not alter the number of brood masses produced and hence the amount of reproductive effort that was allocated to egg production. Therefore, our finding that female survival was increased when receiving paternal assistance provides, to our knowledge, the first definitive evidence that maternal care reduces female lifespan. These results are of major importance to theoretical models on the evolution of parental care.     

Maternal influences on brood sex ratios: an experimental study in tree swallows

When the reproductive value of sons and daughters differ, parents are expected to adjust the sex ratio of their offspring to produce more of the sex that provides greater fitness returns. The body condition of females or environmental factors, such as food abundance and mate quality, may influence these expected fitness returns. In a previous study of tree swallows (Tachycineta bicolor), we found that females produced more sons in their broods when they were in better body condition (mass corrected for size). We tested this relationship by experimentally clipping some flight feathers to reduce female body condition. As predicted, we found that females with clipped feathers had a lower proportion of sons in their broods and poorer body condition. However, female body condition alone was not a significant predictor of brood sex ratio in our experiment. We suggest that brood sex ratio is causally related to some other factor that covaries with body condition, most likely the foraging ability of females. The hypothesis that brood sex ratios are influenced by individual differences in female foraging ability is supported by a high repeatability of brood sex ratio for individual females. Thus, maternal effects may have a strong influence on the sex ratios of offspring.     

A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude,depth, salinity and superfamily

Life history traits (mean and maximum body length of females, number of embryos per brood = brood size, embryo diameter, number of broods per female, lifespan of females) for 302 populations of aquatic gammaridean amphipods, representing 214 species in 16 superfamilies, were reviewed. The variation of these traits, of lifetime potential fecundity (i.e. the number of embryos produced per female lifespan) and of reproductive potential (i.e. the number of embryos produced per female per year), with temperature (latitude), depth, salinity and superfamily, was investigated by various univariate and multivariate methods. Gammaridean amphipods comprise semelparous and iteroparous populations and species, with semiannual, annual, biannual or perennial life cycles. However, most gammarideans studied so far are iteroparous annuals. Body length explains most of the variation in brood size and embryo diameter. The reproductive potential may be increased by increasing body size for a constant breeding frequency, by increasing brood size at the expense of smaller embryos, by increasing breeding frequency for a constant lifespan at the expense of smaller individual broods and/or embryos, and by increasing longevity for a constant breeding frequency and brood size. Combinations of these different options constitute the life history patterns of gammarideans, which vary across superfamilies, latitude and depth, and cannot simply be explained by variations in body length. High latitude species were generally characterized by biannual or perennial life histories, large body size, delayed maturity, and single or few broods with many, relatively large embryos; converse sets of traits characterized low latitude species. Deep-living species had relatively smaller broods and embryos than their shallow-living relatives, yet did not produce more broods. However, different superfamilies dominated in different habitats. The importance of natural selection relative to phylogenetic (historical) and physiological constraints in the forging of these patterns is discussed.     

Reproductive correlates of plumage coloration of female Mountain Bluebirds

Many studies have shown that the plumage coloration of male birds can act as an honest signal of quality, indicating benefits that a female could gain from pairing with a specific male. In some species, females also display ornamental plumage, but less is known about the function and potential adaptive significance of female coloration because most research has focused on male coloration. Male Mountain Bluebirds (Sialia currucoides) display full body, ultraviolet (UV)‐blue plumage, whereas female plumage is more subdued, with blue color focused on the rump, wing, and tail. During the 2011 and 2012 breeding seasons (May–July) near Kamloops, BC, Canada, we examined coloration of the rump and tail of female Mountain Bluebirds to determine if their plumage could act as an indicator of direct reproductive benefits (e.g., enhanced parental care or reproductive success) to potential mates. We found no relationship between female plumage coloration and either provisioning rate or fledging success. However, female coloration varied with age, with after‐second‐year (ASY) females having brighter, more UV‐blue tail feathers than second‐year (SY) females. In addition, ASY females with brighter, more UV‐blue tails had larger clutches. We also observed positive assortative mating by tarsus length. Because previous work with other species suggests that female body size may be a good predictor of breeding success, males could potentially benefit from pairing with larger females. However, reproductive success did not vary with female size in our study. Although our evidence that structural plumage coloration of female Mountain Bluebirds is a signal of direct reproductive benefits for males (e.g., higher reproductive success) is limited, our results (i.e., ASY females with brighter tails than SY females, and ASY females with brighter tails having larger clutches) do suggest the potential for sexual selection to act on female coloration.     

Sexual dimorphism and growth trade‐offs in Blue Tit Cyanistes caeruleus nestlings

The outcome of sibling competition for food is often determined by variation in body size within the brood and involves trade‐offs; traits that enhance competitive ability within the nest may be developed at the expense of traits that enable effective flight at fledging, or vice versa. We quantified growth of skeletal, body mass and feather traits in male and female Blue Tit Cyanistes caeruleus nestlings. Males were significantly heavier, had longer tarsi and tended to have greater head–bill lengths than females, whereas females were similar to males in wing flight feather growth. These differences in growth may result from sexual differences in selection of the traits. Females are likely to prioritize feather growth to facilitate synchronized fledging with the rest of the brood, and to enhance escape from predators. We suggest that males are heavier and develop longer tarsi because body size is an important determinant of male reproductive success.     

Effects of within‐colony competition on body size asymmetries and reproductive skew in a social spider

Reproductive partitioning is a key component of social organization in groups of cooperative organisms. In colonies of permanently social spiders of the genus Stegodyphus less than half of the females reproduce, while all females, including nonreproducers, perform suicidal allo‐maternal care. Some theoretical models suggest that reproductive skew is a result of contest competition within colonies, leading to size hierarchies where only the largest females become reproducers. We investigated the effect of competition on within‐group body size variation over six months in S. dumicola, by manipulating food level and colony size. We found no evidence that competition leads to increased size asymmetry within colonies, suggesting that contest competition may not be the proximate explanation for reproductive skew. Within‐colony body size variation was high already in the juvenile stage, and did not increase over the course of the experiment, suggesting that body size variation is shaped at an early stage. This might facilitate task specialization within colonies and ensure colony‐level reproductive output by early allocation of reproductive roles. We suggest that reproductive skew in social spiders may be an adaptation to sociality selected through inclusive fitness benefits of allo‐maternal care as well as colony‐level benefits maximizing colony survival and production.     

Shared care provides time-budgeting advantages for female eiders

Shared parental care resulting from brood amalgamation is often considered beneficial to parents. However, the benefit of grouping (a decline in individual vigilance despite an increase in collective vigilance, with a concomitant increase in individual feeding time) has not been evoked as a factor promoting shared care. Eider females, Somateria mollissima, are subject to substantial energetic costs during breeding, and sometimes share brood-rearing duties. We compared the activity budgets and feeding behaviour of lone tenders and multifemale tenders. We also measured the collective vigilance of multifemale tenders and examined whether the coordination of feeding activity among females changes with time. As expected, the proportion of time spent feeding increased, and the proportion of time spent vigilant decreased, as the number of females attending the brood increased. None the less, the collective vigilance of multifemale tenders was at least 20% higher than the vigilance of lone tenders. Furthermore, multifemale tending allowed females to feed more optimally, as dive duration increased with the number of females tending the brood. The level of parental investment by individual females after hatching of the eggs is therefore related to the number of tending females and, based on previous work, a female's body condition when the eggs hatch is also logically connected with the number of tending females. Whether females sharing brood care on a permanent basis coordinate their feeding activity, so as to increase the potential protection of ducklings against predation, remains equivocal. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Group composition affects male reproductive partitioning in a cooperatively breeding cichlid

Individuals within groups of cooperatively breeding species may partition reproduction, with the dominant pair often taking the largest share. The dominant's ability to reproductively control subordinates may depend on differences in competitive ability, due to, e.g. body size differences, but may also depend on the number of same‐sex competitors inside the group. We tested experimentally whether subordinates reproduce more when these subordinates are large or when a second subordinate of the same sex need to be controlled by the dominants, using the cooperatively breeding cichlid Neolamprologus pulcher. Dominant pairs were assisted by a large and a small unrelated subordinate; sexes of these fish were varied in a full‐factorial design (giving four treatments). Dominant males lost significantly more parentage to the large subordinate male when a small subordinate male was also present, compared to when a small subordinate female was present. However, subordinate paternity was generally low and did not significantly curb total dominant male reproductive output, which was more affected by the sizes and numbers of reproductive females present inside his group. Dominant female maternity, clutch sizes and total output did not depend on the treatments. Subordinate–subordinate reproduction was virtually absent (one out of 874 offspring). Female subordinates were more likely to provide care for their own broods. In contrast, male subordinates did not adjust their level of care to their parentage. Variability in female subordinate alloparental brood care was particularly high, with females showing more care than males in general. We also detected effects of growth rate and food ration on parentage independent of the treatments, most notably: (i) a trade‐off between dominant male growth rate and paternity; (ii) a decrease in dominant male paternity with increasing food ration; (iii) a positive effect of growth rate on paternity in small males. We conclude that dominant males should be sensitive to the number and sizes of subordinate males present in their group, particularly when these subordinates are not helpful or grow fast, and food is plentiful. Dominant females should be less sensitive, because female subordinates do not appear to impose reproductive costs and can be helpful through alloparental brood care.     

Variation in selection pressure acting on body size by age and sex in a reverse sexual size dimorphic raptor

Body size strongly influences fitness, with larger individuals benefiting in terms of both greater productivity and survivorship; for reverse sexual size dimorphic (RSD) species, this relationship may be more complex. We examined the selection pressures acting on body size in male and female Merlins Falco columbarius to assess whether larger or smaller individuals of this RSD species were favoured in terms of survival and breeding performance. For males and females there were clear links between body size and survival but the exact relationship varied by sex. Among males, birds that survived each year class were larger than those that died and yearlings were on average smaller than older birds, but there were no measurable differences among adult males (age 2+). Among females, larger individuals aged 1 and 2 years were more likely to survive, but this size‐based pattern was not apparent in older age classes. Size early in life predicted the lifespan in male Merlins but not as strongly as for females and not for the largest individuals. Reproductive performance based on brood size was not associated with body size in either males or females, but there was a weak positive relationship between female body size and lifetime reproductive success. Selection appears to favour larger males and females but there is no indication that the population is evolving towards bigger individuals, perhaps in part due to selection against the largest birds. Increased survival may allow larger and higher quality individuals to occupy higher quality territories as they age and thereby to accrue greater lifetime reproductive success in the process.     

The biology of Brevineura froggatti and phylogenetic conservatism in Australian allodapine bees (Apidae,Allodapini)

Summary: We present the first data on the social biology of the allodapine bee, Brevineura froggatti. Colony sizes are small, and only 12.5% of nests contained more than two females. Brood rearing occurs throughout the year, including winter, as it does in the other species of Brevineura studied to date. In both Brevineura species, per capita brood production is much higher in multi-female nests than single female nests, raising the question of why more colonies aren't multifemale. The occurrence of small colony sizes, despite large benefits to group living, differs strongly from species of the sister clade Exoneura. These findings, combined with previous allodapine studies, indicate conservatism in voltinism, brood phenology and colony size within, but not between, Australian allodapine genera.     

Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

Why make daughters larger? Maternal sex-allocation and sex-dependent selection for body size in a mass-provisioning wasp, Trypoxylon politum

Mass-provisioning wasps package maternal investment into broodcells, sealed structures that contain all the provisions necessaryfor an offspring's growth and development. Optimal sex-allocationtheory predicts that if maternal provisions determine the sizeof each offspring, and the amount of provisions available toeach offspring varies, females should allocate well-stockedbrood cells to the sex that benefits most from being large.I tested this hypothesis using observations of organ-pipe wasps,Trypoxylon politum, and dissections of their nests. A Mississippipopulation of T. politum was intensively studied from 1993 to1995. This population fit the assumptions of optimal sex-allocationmodels by Green and Brockmann and Grafen. Female weight at emergencewas 1.29 times that of males, and wing length was 1.15 timesthat of males. This discrepancy in size occurred because thevolume of parental provisions strongly influenced adult bodysize, and better-stocked brood cells were preferentially allocatedto daughters. Brood-cell volume correlated with both wing lengthand weight at emergence in both sexes, and the chance that agiven brood cell contained a female offspring increased withincreasing brood-cell volume. Fitness was positively relatedto body size for females, but I found no evidence of an advantageto large males. Although there was evidence of stabilizing selectionfor male wing length in one year, there was no evidence of anincreasing relationship between body size and fitness (directionalselection) for males in either 1993 or 1994. Female fecunditywas positively related to body size in both years, indicatingthat larger females have increased reproductive success. Therate at which females provisioned brood cells was also correlatedwith body size. Observed patterns of investment in brood cellsare quantitatively consistent with the predictions of optimalsex-allocation theory, but certain aspects of female provisioningbehavior suggest females are not following a single "optimal"strategy. Patterns of provisioning were variable among differentfemales at the study site during the same year. Large femalestended to produce larger offspring. Although Brockmann and Grafen'smodel predicts a single, population wide "switchpoint" fromthe production of male to female offspring, there was no evidencefor such a switchpoint