Brood sex ratio varies with diet composition in a generalist raptor

While sex allocation has been investigated productively at both population and family levels, as yet no general theory has been developed that is capable of linking processes at these two ecological scales, and very few empirical studies have examined cross‐scale patterns. In Finnish northern goshawks (Accipiter gentilis), nestling sex ratio of local subpopulations is related to the spatial and temporal variation in the abundance of their principal avian prey, woodland grouse. Using data from an urban breeding population in Hamburg, Germany, I investigated: (1) whether brood sex ratio of goshawks varies with diet composition at the family level; (2) whether such variation could reflect adaptive adjustment; and (3) how family‐level allocation can drive population‐level patterns, such as those observed in Finland. Feral pigeons (Columba livia) were the most important prey species, with a pooled contribution to total diet of 36%. Brood sex ratio varied significantly with the proportion of pigeons in the breeding‐season diet of pairs (increasing male bias). However, there was no evidence for sex‐differential effects of diet composition, so it remains unclear whether the observed sex‐ratio variation was an adaptive response. As all study pairs inhabited an (urban) environment where pigeons were unusually abundant, family‐level sex‐ratio adjustment caused a marked male bias in offspring sex ratio at the population level (male‐biased nestling sex ratio in four of five years; pooled data: 60% males). This suggests that the large‐scale variation observed in Finnish goshawk populations mirrors sex‐ratio adjustment shown by individual families in response to small‐scale environmental conditions. Apart from linking patterns empirically across ecological scales, this study is, to my knowledge, the first to demonstrate that family‐level brood sex ratio varies with realized resource use (diet composition) in a raptor species. Previous studies either failed to find significant associations or, more commonly, violated theoretical assumptions by measuring environmental prey abundance (often integrated over large areas) rather than realized prey use of individual breeding pairs. I conducted a meta‐analysis of offspring sex‐ratio data from 17 goshawk populations across Europe to put my results into perspective. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 937–951.     

Digest: Evolution of eusociality favored by split sex ratios under worker-control*

Eusociality has repeatedly independently evolved in ants, bees, and wasps (Hymenoptera), leading to the idea that haplodiploidy may be an important driving factor in this group. Using a modeling approach, Quiñones et al. show that split sex ratios and worker control of sex ratios (achieved by removal of male brood) can promote the initial evolution of helping raise offspring of related individuals. However, over time, these factors can result in social polymorphism, that is, a mix of solitary and social nests, or to eusocial colonies with three different strategies, namely those that produce mostly females, mostly males, or a balanced sex ratio.     

Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee, Bombus terrestris

Brain and behavioural lateralization at the population level has been recently hypothesized to have evolved under social selective pressures as a strategy to optimize coordination among asymmetrical individuals. Evidence for this hypothesis have been collected in Hymenoptera: eusocial honey bees showed olfactory lateralization at the population level, whereas solitary mason bees only showed individual-level olfactory lateralization. Here we investigated lateralization of odour detection and learning in the bumble bee, Bombus terrestris L., an annual eusocial species of Hymenoptera. By training bumble bees on the proboscis extension reflex paradigm with only one antenna in use, we provided the very first evidence of asymmetrical performance favouring the right antenna in responding to learned odours in this species. Electroantennographic responses did not reveal significant antennal asymmetries in odour detection, whereas morphological counting of olfactory sensilla showed a predominance in the number of olfactory sensilla trichodea type A in the right antenna. The occurrence of a population level asymmetry in olfactory learning of bumble bee provides new information on the relationship between social behaviour and the evolution of population-level asymmetries in animals.     

Recombination,chromosome number and eusociality in the Hymenoptera

Extraordinarily high rates of recombination have been observed in some eusocial species. The most popular explanation is that increased recombination increases genetic variation among workers, which in turn increases colony performance, for example by increasing parasite resistance. However, support for the generality of higher recombination rates among eusocial organisms remains weak, due to low sample size and a lack of phylogenetic independence of observations. Recombination rate, although difficult to measure directly, is correlated with chromosome number. As predicted, several authors have noted that chromosome numbers are higher among the eusocial species of Hymenoptera (ants, bees and wasps). Here, we present a formal comparative analysis of karyotype data from 1567 species of Hymenoptera. Contrary to earlier studies, we find no evidence for an absolute difference between chromosome number in eusocial and solitary species of Hymenoptera. However, we find support for an increased rate of chromosome number change in eusocial taxa. We show that among eusocial taxa colony size is able to explain some of the variation in chromosome number: intermediate‐sized colonies have more chromosomes than those that are either very small or very large. However, we were unable to detect effects of a number of other colony characteristics predicted to affect recombination rate – including colony relatedness and caste number. Taken together, our results support the view that a eusocial lifestyle has led to variable selection pressure for increased recombination rates, but that identifying the factors contributing to this variable selection will require further theoretical and empirical effort.     

Fluorescence in situ hybridization: a new method for determining primary sex ratio in ants

The haplodiploid sex determining system in Hymenoptera, whereby males develop from haploid eggs and females from diploid eggs, allows females to control the primary sex ratio (the proportion of each sex at oviposition) in response to ecological and/or genetic conditions. Surprisingly, primary sex ratio adjustment by queens in eusocial Hymenoptera has been poorly studied, because of difficulties in sexing the eggs laid. Here, we show that fluorescence in situ hybridization (FISH) can be used to accurately determine the sex (haploid or diploid) of eggs, and hence the primary sex ratio, in ants. We first isolated the homologue coding sequences of the abdominal-A gene from 10 species of 8 subfamilies of Formicidae. Our data show that the nucleotide sequence of this gene is highly conserved among the different subfamilies. Second, we used a sequence of 4.5 kbp from this gene as a DNA probe for primary sex ratio determination by FISH. Our results show that this DNA probe hybridizes successfully with its complementary DNA sequence in all ant species tested, and allows reliable determination of the sex of eggs. Our proposed method should greatly facilitate empirical tests of primary sex ratio in ants.     

Social polymorphism in the sweat bee <Emphasis Type="Italic">Lasioglossum (Evylaeus) baleicum</Emphasis> (Cockerell) (Hymenoptera,Halictidae) in Hokkaido,northern Japan

Summary The life cycle and social behaviour of the sweat bee Lasioglossum (Evylaeus) baleicum (Cockerell) was investigated in two geographically separate populations in Hokkaido, northern Japan. Colonies were excavated throughout the brood rearing season from an aggregation in Nishioka forest park, Sapporo, and near Kawakita in eastern Hokkaido during 2000 and 2001. The Nishioka population produced two discrete broods during the year and was weakly eusocial; 57% of workers were mated and 28% exhibited some ovarian development, 12–16% of the first brood was male, and workers were on average 4.5% smaller than their respective queen. In contrast, the population at Kawakita was solitary, and produced a single brood per year with an unbiased sex ratio. In addition however, there were some solitary colonies in the Nishioka population and evidence of a partial second brood in some colonies at Kawakita, suggesting differences between the populations are not fixed and that this species is truly socially polymorphic. L. (E.) baleicum is a member of the fulvicorne species group, which includes other examples of social polymorphic species as well as solitary and eusocial species, though this is the only species of this group so far known to exhibit a solitary/non-delayed eusocial polymorphism. Recent studies suggest that social polymorphism has both genetic and environmental influences, raising questions as to the relative import of each.     

Adaptive colony sex ratios in primitively eusocial bees

Colony-level predictions about sex-ratio optimization in eusocial Hymenoptera are different from the ones that apply to the population level. A recent empirical study on the sweat bee Halictus rubicundus has revealed a distinct pattern in the colony sex ratio of the summer brood: eusocial colonies produced more female-biased sex ratios and non-eusocial colonies produce more male-biased sex ratios. These data are consistent with theoretical hypotheses as put forward by Trivers and Hare and several later authors. When interpreted in the light of these theoretical contentions, the sex-ratio variation in Halictus rubicundus appears to be adaptive for workers, replacement queens and - under reasonable additional assumptions - also for foundresses.     

Honey bee queen mandibular pheromone inhibits ovary development and fecundity in a fruit fly

A key feature of eusocial insects is their reproductive division of labour. The queen signals her fecundity to her potentially reproductive daughters via a pheromone, which renders them sterile. In contrast, solitary insects lack division in reproductive labour and there is no such social signalling or need for ovary‐regulating pheromones. Nonetheless, females from both non‐social and eusocial lineages are expected to regulate their ovaries to maximize inclusive lifetime reproductive success. It is not known, however, whether the underlying networks that regulate ovary activation are homologous between non‐social and eusocial taxa, especially when these taxa are phylogenetically distant. In this study, we provide evidence that solitary fruit flies may share a conserved ovary‐regulating pathway with a eusocial honey bee, Apis mellifera L. (Hymenoptera: Apidae). Specifically, we demonstrate that honey bee queen mandibular pheromone (QMP) inhibits fly ovaries in much the same way as it suppresses worker ovaries. Drosophila melanogaster Meigen (Diptera: Drosophilidae) exposed to sufficient doses of QMP showed a reduction in ovary size, produced fewer eggs, and generated fewer viable offspring, relative to unexposed controls. Drosophila melanogaster therefore responds to an interspecific social cue to which it would not normally be exposed. Although we cannot strictly rule out an incidental effect, this conspicuous response suggests that these two species may share an underlying mechanism for ovary regulation. Why a non‐social species of fly responds to a highly social bee's pheromone is not clear, but one possibility is that solitary and social insects share pathways associated with female reproduction, as predicted by the ‘groundplan’ hypothesis of social evolution.     

The marine side of a terrestrial carnivore: intra-population variation in use of allochthonous resources by arctic foxes

Inter-individual variation in diet within generalist animal populations is thought to be a widespread phenomenon but its potential causes are poorly known. Inter-individual variation can be amplified by the availability and use of allochthonous resources, i.e., resources coming from spatially distinct ecosystems. Using a wild population of arctic fox as a study model, we tested hypotheses that could explain variation in both population and individual isotopic niches, used here as proxy for the trophic niche. The arctic fox is an opportunistic forager, dwelling in terrestrial and marine environments characterized by strong spatial (arctic-nesting birds) and temporal (cyclic lemmings) fluctuations in resource abundance. First, we tested the hypothesis that generalist foraging habits, in association with temporal variation in prey accessibility, should induce temporal changes in isotopic niche width and diet. Second, we investigated whether within-population variation in the isotopic niche could be explained by individual characteristics (sex and breeding status) and environmental factors (spatiotemporal variation in prey availability). We addressed these questions using isotopic analysis and Bayesian mixing models in conjunction with linear mixed-effects models. We found that: i) arctic fox populations can simultaneously undergo short-term (i.e., within a few months) reduction in both isotopic niche width and inter-individual variability in isotopic ratios, ii) individual isotopic ratios were higher and more representative of a marine-based diet for non-breeding than breeding foxes early in spring, and iii) lemming population cycles did not appear to directly influence the diet of individual foxes after taking their breeding status into account. However, lemming abundance was correlated to proportion of breeding foxes, and could thus indirectly affect the diet at the population scale.     

Variable coloration is associated with dampened population fluctuations in noctuid moths

Theory and recent reviews state that greater genetic and phenotypic variation should be beneficial for population abundance and stability. Experimental evaluations of this prediction are rare, of short duration and conducted under controlled environmental settings. The question whether greater diversity in functionally important traits stabilizes populations under more complex ecological conditions in the wild has not been systematically evaluated. Moths are mainly nocturnal, with a large variation in colour patterns among species, and constitute an important food source for many types of organisms. Here, we report the results of a long-term (2003–2013) monitoring study of 115 100 noctuid moths from 246 species. Analysis of time-series data provide rare evidence that species with higher levels of inter-individual variation in colour pattern have higher average abundances and undergo smaller between-year fluctuations compared with species having less variable colour patterns. The signature of interspecific temporal synchronization of abundance fluctuations was weak, suggesting that the dynamics were driven by species-specific biotic interactions rather than by some common, density-independent factor(s). We conclude that individual variation in colour patterns dampens population abundance fluctuations, and suggest that this may partly reflect that colour pattern polymorphism provides protection from visually oriented predators and parasitoids.     

Shared reproduction and sex ratio adjustment to clutch size in a socially polymorphic orchid bee

Nests of the primitively eusocial orchid bee Euglossa viridissima are generally founded by a solitary female but can be reactivated by female offspring, in the presence or absence of the mother. The population therefore exists of solitary and social nests that co-occur in an area. A female can stay as a subordinate helper under a dominant female or disperse to become a solitary foundress. Yet, the costs and benefits of the different social phenotypes are so far little understood. Here, we compared solitary and social nests of orchid bees. We used offspring of solitary and social nests to calculate offspring sex ratio, and applied molecular markers to calculate intranidal relatedness, infer maternity and test whether sociality may have a genetic component. We found that social nests had on average more brood than solitary nests. The overall sex ratio in the population did not differ from 1:1. However, social nests tended to produce a split sex ratio with some nests producing mainly males and others mainly female offspring. Regardless of social phenotype, the number of offspring was correlated with the sex ratio, with smaller nests having a more female-biased offspring. In social nests, not all offspring resulted from a single-mated mother, which was also the case for some solitary nests. This suggests shared reproduction in social nests and may be an indication that intraspecific parasitism and nest takeover are not uncommon. Structure analyses did not reveal different genetic background of the two social phenotypes. Our results suggest that there is no clear benefit that favours one of the two social phenotypes over the other and that the population is kept at balance in terms of sex ratio.     

Effective population size in eusocial Hymenoptera with worker-produced males

In many eusocial Hymenoptera, a proportion of males are produced by workers. To assess the effect of male production by workers on the effective population size N_e, a general expression of N_e in Hymenoptera with worker-produced males is derived on the basis of the genetic drift in the frequency of a neutral allele. Stochastic simulation verifies that the obtained expression gives a good prediction of N_e under a wide range of conditions. Numerical computation with the expression indicates that worker reproduction generally reduces N_e. The reduction can be serious in populations with a unity or female-biased breeding sex ratio. Worker reproduction may increase N_e in populations with a male-biased breeding sex ratio, only if each laying worker produce a small number of males and the difference of male progeny number among workers is not large. Worker reproduction could be an important cause of the generally lower genetic variation found in Hymenoptera, through its effect on N_e.     

Variable queen number in ant colonies: no impact on queen turnover, inbreeding, and population genetic differentiation in the ant Formica selysi

Variation in queen number alters the genetic structure of social insect colonies, which in turn affects patterns of kin-selected conflict and cooperation. Theory suggests that shifts from single- to multiple-queen colonies are often associated with other changes in the breeding system, such as higher queen turnover, more local mating, and restricted dispersal. These changes may restrict gene flow between the two types of colonies and it has been suggested that this might ultimately lead to sympatric speciation. We performed a detailed microsatellite analysis of a large population of the ant Formica selysi, which revealed extensive variation in social structure, with 71 colonies headed by a single queen and 41 by multiple queens. This polymorphism in social structure appeared stable over time, since little change in the number of queens per colony was detected over a five-year period. Apart from queen number, single- and multiple-queen colonies had very similar breeding systems. Queen turnover was absent or very low in both types of colonies. Single- and multiple-queen colonies exhibited very small but significant levels of inbreeding, which indicates a slight deviation from random mating at a local scale and suggests that a small proportion of queens mate with related males. For both types of colonies, there was very little genetic structuring above the level of the nest, with no sign of isolation by distance. These similarities in the breeding systems were associated with a complete lack of genetic differentiation between single- and multiple-queen colonies, which provides no support for the hypothesis that change in queen number leads to restricted gene flow between social forms. Overall, this study suggests that the higher rates of queen turnover, local mating, and population structuring that are often associated with multiple-queen colonies do not appear when single- and multiple-queen colonies still coexist within the same population, but build up over time in populations consisting mostly of multiple-queen colonies.     

Convergent evolution in social swallows (Aves: Hirundinidae)

Behavioral shifts can initiate morphological evolution by pushing lineages into new adaptive zones. This has primarily been examined in ecological behaviors, such as foraging, but social behaviors may also alter morphology. Swallows and martins (Hirundinidae) are aerial insectivores that exhibit a range of social behaviors, from solitary to colonial breeding and foraging. Using a well‐resolved phylogenetic tree, a database of social behaviors, and morphological measurements, we ask how shifts from solitary to social breeding and foraging have affected morphological evolution in the Hirundinidae. Using a threshold model of discrete state evolution, we find that shifts in both breeding and foraging social behavior are common across the phylogeny of swallows. Solitary swallows have highly variable morphology, while social swallows show much less absolute variance in all morphological traits. Metrics of convergence based on both the trajectory of social lineages through morphospace and the overall morphological distance between social species scaled by their phylogenetic distance indicate strong convergence in social swallows, especially socially foraging swallows. Smaller physical traits generally observed in social species suggest that social species benefit from a distinctive flight style, likely increasing maneuverability and foraging success and reducing in‐flight collisions within large flocks. These results highlight the importance of sociality in species evolution, a link that had previously been examined only in eusocial insects and primates.     

The genomic impact of 100 million years of social evolution in seven ant species

Ants (Hymenoptera, Formicidae) represent one of the most successful eusocial taxa in terms of both their geographic distribution and species number. The publication of seven ant genomes within the past year was a quantum leap for socio- and ant genomics. The diversity of social organization in ants makes them excellent model organisms to study the evolution of social systems. Comparing the ant genomes with those of the honeybee, a lineage that evolved eusociality independently from ants, and solitary insects suggests that there are significant differences in key aspects of genome organization between social and solitary insects, as well as among ant species. Altogether, these seven ant genomes open exciting new research avenues and opportunities for understanding the genetic basis and regulation of social species, and adaptive complex systems in general.     

Sex allocation in the ant Camponotus (Colobopsis) nipponicus (Wheeler): II. The effect of resource availability on sex-ratio variability

Sex-ratio studies have played a prominent role in tests of kin selection theory in the eusocial Hymenoptera. The winner in sex-ratio conflict between queens and workers must control the ratio through proximate mechanisms. To determine how a colony adjusts its sex ratio, the mechanism of sex-ratio determination was analyzed in the field in colonies of the ant Camponotus (Colobopsis) nipponicus. A path model including five colony characteristics showed that the resource availability of the colony (quantified as the amount of stored fat in the bodies of the workers) has a large positive effect on the proportion of new queens in the female larvae, but has little effect on male production. The results indicated that a colony adjusts the sex ratio by altering the proportion of new queens obtained from a diploid brood in response to resource availability rather than by eliminating male larvae.     

Variation in nest-site occupancy and breeding outcome in a threatened Subantarctic raptor

Breeding outcome in birds can be influenced by both intrinsic and extrinsic factors, which may contribute differentially to each stage of the breeding cycle. Island raptors are relatively threatened species that rely on simplified food webs and usually co-occur with invasive species. Here, we studied a population of Striated Caracara Phalcoboenus australis in Isla de los Estados (Argentina) to understand the relative contribution of food availability, topographical features and territoriality to breeding parameters. Caracaras in the area depend on the short seasonal (i.e. pulsed) availability of seabirds for feeding their chicks. On the other hand, the recent introduction of non-native ungulates may have led to a suboptimal breeding environment by reducing Caracara nest-site availability within the seabird colonies via disturbance of the grassland. Using data from seven breeding seasons we analyse the abundance, the proportion of breeding individuals, the spatial structure of breeding events and the population-level breeding performance, including chick sex ratio, to study whether the breeding ecology of this species is still shaped by marine food web pulses or could be associated with invasive herbivore disturbance. The breeding adults represented only 6–15% of the population. The spatial pattern of nest-sites did not differ from random arrangement after considering the heterogeneous distribution of food availability. Territory identity accounted for most of the variation in clutch size and productivity, and penguin availability explained part of the variability in territory occupancy and hatching rate. The chick sex ratio was biased towards females and varied according to brood size, with the more productive territories producing 91% of males. The breeding cycle of this population is still mainly dependent upon the Rockhopper Penguin Eudyptes chrysocome food pulse and presents mixed evidence of being disrupted by invasive herbivores. The studied factors contributed differentially to the output of each reproductive stage, with territory identity accounting for most of the variation. Our results suggest that individual-level, long-term data could be relevant to understanding the dynamics of this species in the Fuegian archipelago, and thus a broad-scale research programme is warranted to assess the conservation status and propose future management scenarios for this species.     

Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis

In primitively eusocial insects, caste expression is flexible. Even though Polistes species are well known to show social trait variation (e.g., worker vs. gyne) depending on ecological context, loss of worker caste in some populations of a eusocial, worker-containing species has never been documented. We report first data on geographic variation in caste expression in Polistes biglumis. We compared physiological and behavioural traits of the first female offspring from four populations that experience different climatic conditions and social parasite prevalence. We demonstrated that the first female offspring to emerge in cold areas with high parasite prevalence had more abundant, gyne-like fat bodies and exhibited lower foraging effort, in comparison to the first female offspring produced in warm areas with low parasite prevalence. Thus, the populations under severe environmental conditions produced a totipotent female offspring and suppressed worker production, whereas the population living in less extreme environmental conditions produced worker-like females as first female offspring and gyne-like females as offspring that emerged later. The existence of mixed social strategies among populations of primitively eusocial species could have important consequences for the study of social evolution, shedding light on the sequence of steps by which populations evolve between the extremes of solitary state and eusocial state.     

Ecological generalism facilitates the evolution of sociality in snapping shrimps

Evidence from insects and vertebrates suggests that cooperation may have enabled species to expand their niches, becoming ecological generalists and dominating the ecosystems in which they occur. Consistent with this idea, eusocial species of sponge‐dwelling Synalpheus shrimps from Belize are ecological generalists with a broader host breadth and higher abundance than non‐eusocial species. We evaluate whether sociality promotes ecological generalism (social conquest hypothesis) or whether ecological generalism facilitates the transition to sociality (social transition hypothesis) in 38 Synalpheus shrimp species. We find that sociality evolves primarily from host generalists, and almost exclusively so for transitions to eusociality. Additionally, sponge volume is more important for explaining social transitions towards communal breeding than to eusociality, suggesting that different ecological factors may influence the independent evolutionary origins of sociality in Synalpheus shrimps. Ultimately, our results are consistent with the social transition hypothesis and the idea that ecological generalism facilitates the transition to sociality.     

Reproductive parameters vary with social and ecological factors in the polygynous ant Formica exsecta

Due to their haplo‐diploid sex determination system and the resulting conflict over optimal sex allocation between queens and workers, social Hymenoptera have become important model species to study variation in sex allocation. While many studies indeed reported sex allocation to be affected by social factors such as colony kin structure or queen number, others, however, found that sex allocation was impacted by ecological factors such as food availability. In this paper, we present one of the rare studies that simultaneously investigated the effects of social and ecological factors on social insect nest reproductive parameters (sex and reproductive allocation, nest productivity) across several years. We found that the sex ratio was extremely male biased in a polygynous (multiple queens per nest) population of the ant Formica exsecta. Nest‐level sex allocation followed the pattern predicted by the queen‐replenishment hypothesis, which holds that gynes (new queens) should only be produced and recruited in nests with low queen number (i.e. reduced local resource competition) to ensure nest survival. Accordingly, queen number (social factor) was the main determinant on whether a nest produced gynes or males. However, ecological factors had a large impact on nest productivity and therefore on a nest's resource pool, which determines the degree of local resource competition among co‐breeding queens and at what threshold in queen number nests should switch from male to gyne production. Additionally, our genetic data revealed that gynes are recruited back to their parental nests after mating. However, our genetic data are also consistent with some adult queens dispersing on foot from nests where they were produced to nests that never produced queens. As worker production is reduced in gyne‐producing nests, queen migration might be offset by workers moving in the other direction, leading to a nest network characterized by reproductive division of labour. Altogether our study shows that both, social and ecological factors can influence long‐term nest reproductive strategies in insect societies.