The evolution of morphological castes under decoupled control.

Eusociality, where units that previously reproduced independently function as one entity, is of major interest in evolutionary biology. Obligate eusociality is characterized by morphologically differentiated castes and reduced conflict. We explore conditions under which morphological castes may arise in the Hymenoptera and factors constraining their evolution. Control over offspring morphology and behaviour seems likely to be decoupled. Provisioners (queens and workers) can influence offspring morphology directly through the nutrition they provide, while adult offspring control their own behaviour. Provisioners may, however, influence worker behaviour indirectly if offspring modify their behaviour in response to their morphology. If manipulation underlies helping, we should not see helping evolve before specialized worker morphology, yet empirical observations suggest that behavioural castes precede morphological castes. We use evolutionary invasion analyses to show how the evolution of a morphologically differentiated worker caste depends on the prior presence of a behavioural caste: specialist worker morphology will be mismatched with behaviour unless some offspring already choose to work. A mother's certainty about her offspring's behaviour is also critical-less certainty results in greater mismatch. We show how baseline worker productivity can affect the likelihood of a morphological trait being favoured by natural selection. We then show how under a decoupled control scenario, morphologically differentiated castes should be less and less likely to be lost as they become more specialized. We also suggest that for eusociality to be evolutionarily irreversible, workers must be unable to functionally replace reproductives and reproductives must be unable to reproduce without help from workers.

Brood Parasites That Care: Alternative Nesting Tactics in a Subsocial Wasp.

AbstractHosts and brood parasites are a classic example of conflict. Parasites typically provide no offspring care after laying eggs, imposing costs on hosts. Female subsocial wasps (Ammophila pubescens) alternate between initiating their own nests and using an "intruder" tactic of replacing eggs in nests of unrelated conspecifics. Hosts can respond by substituting new eggs of their own, with up to eight reciprocal replacements. Remarkably, intruders usually provision offspring in host nests, often alongside hosts. We used field data to investigate why intruders provision and to understand the basis of interactions. We found that intruders could not increase their fitness payoffs by using the typical brood parasite tactic of not provisioning offspring. Intruders using the typical tactic would benefit when hosts provisioned in their stead, but their offspring would starve when hosts failed to provision. Although some hosts obtained positive payoffs when intruders mistakenly provisioned their offspring, on average utilizing a conspecific nest represents parasitism: hosts pay costs while intruders benefit. Hosts and intruders used the same tactic of egg replacement, but intruders more often laid the final egg. Selection should favor better discrimination of offspring, which could lead to repeated cycles of costly egg replacement.

Multicenter, multidisciplinary user-centered design of a clinical decision-support and simulation system for massive transfusion.

BACKGROUND: Managing critical bleeding with massive transfusion (MT) requires a multidisciplinary team, often physically separated, to perform several simultaneous tasks at short notice. This places a significant cognitive load on team members, who must maintain situational awareness in rapidly changing scenarios. Similar resuscitation scenarios have benefited from the use of clinical decision support (CDS) tools. STUDY DESIGN AND METHODS: A multicenter, multidisciplinary, user-centered design (UCD) study was conducted to design a computerized CDS for MT. This study included analysis of the problem context with a cognitive walkthrough, development of a user requirement statement, and co-design with users of prototypes for testing. The final prototype was evaluated using qualitative assessment and the System Usability Scale (SUS). RESULTS: Eighteen participants were recruited across four institutions. The first UCD cycle resulted in the development of four prototype interfaces that addressed the user requirements and context of implementation. Of these, the preferred interface was further developed in the second UCD cycle to create a high-fidelity web-based CDS for MT. This prototype was evaluated by 15 participants using a simulated bleeding scenario and demonstrated an average SUS of 69.3 (above average, SD 16) and a clear interface with easy-to-follow blood product tracking. DISCUSSION: We used a UCD process to explore a highly complex clinical scenario and develop a prototype CDS for MT that incorporates distributive situational awareness, supports multiple user roles, and allows simulated MT training. Evaluation of the impact of this prototype on the efficacy and efficiency of managing MT is currently underway.

Clinical decision support versus a paper-based protocol for massive transfusion: Impact on decision outcomes in a simulation study.

BACKGROUND: Management of major hemorrhage frequently requires massive transfusion (MT) support, which should be delivered effectively and efficiently. We have previously developed a clinical decision support system (CDS) for MT using a multicenter multidisciplinary user-centered design study. Here we examine its impact when administering a MT. STUDY DESIGN AND METHODS: We conducted a randomized simulation trial to compare a CDS for MT with a paper-based MT protocol for the management of simulated hemorrhage. A total of 44 specialist physicians, trainees (residents), and nurses were recruited across critical care to participate in two 20-min simulated bleeding scenarios. The primary outcome was the decision velocity (correct decisions per hour) and overall task completion. Secondary outcomes included cognitive workload and System Usability Scale (SUS). RESULTS: There was a statistically significant increase in decision velocity for CDS-based management (mean 8.5 decisions per hour) compared to paper based (mean 6.9 decisions per hour; p .003, 95% CI 0.6-2.6). There was no significant difference in the overall task completion using CDS-based management (mean 13.3) compared to paper-based (mean 13.2; p .92, 95% CI -1.2-1.3). Cognitive workload was statistically significantly lower using the CDS compared to the paper protocol (mean 57.1 vs. mean 64.5, p .005, 95% CI 2.4-12.5). CDS usability was assessed as a SUS score of 82.5 (IQR 75-87.5). DISCUSSION: Compared to paper-based management, CDS-based MT supports more time-efficient decision-making by users with limited CDS training and achieves similar overall task completion while reducing cognitive load. Clinical implementation will determine whether the benefits demonstrated translate to improved patient outcomes.

Sensory plasticity in a socially plastic bee.

The social Hymenoptera have contributed much to our understanding of the evolution of sensory systems. Attention has focussed chiefly on how sociality and sensory systems have evolved together. In the Hymenoptera, the antennal sensilla are important for optimizing the perception of olfactory social information. Social species have denser antennal sensilla than solitary species, which is thought to enhance social cohesion through nestmate recognition. In the current study, we test whether sensilla numbers vary between populations of the socially plastic sweat bee Halictus rubicundus from regions that vary in climate and the degree to which sociality is expressed. We found population differences in both olfactory and hygro/thermoreceptive sensilla numbers. We also found evidence that olfactory sensilla density is developmentally plastic: when we transplanted bees from Scotland to the south-east of England, their offspring (which developed in the south) had more olfactory hairs than the transplanted individuals themselves (which developed in Scotland). The transplanted bees displayed a mix of social (a queen plus workers) and solitary nesting, but neither individual nor nest phenotype was related to sensilla density. We suggest that this general, rather than caste-specific sensory plasticity provides a flexible means to optimize sensory perception according to the most pressing demands of the environment. Sensory plasticity may support social plasticity in H. rubicundus but does not appear to be causally related to it.

The evolution of eusociality: no risk-return tradeoff but the ecology matters.

The origin of eusociality in the Hymenoptera is a question of major interest. Theory has tended to focus on genetic relatedness, but ecology can be just as important a determinant of whether eusociality evolves. Using the model of Fu et al. (2015), we show how ecological assumptions critically affect the conclusions drawn. Fu et al. inferred that eusociality rarely evolves because it faces a fundamental 'risk-return tradeoff'. The intuitive logic was that worker production represents an opportunity cost because it delays realising a reproductive payoff. However, making empirically justified assumptions that (1) workers take over egg-laying following queen death and (2) productivity increases gradually with each additional worker, we find that the risk-return tradeoff disappears. We then survey Hymenoptera with more specialised morphological castes, and show how the interaction between two common features of eusociality - saturating birth rates and group size-dependent helping decisions - can determine whether eusociality outperforms other strategies.

Biological markets in cooperative breeders: quantifying outside options.

A major aim in evolutionary biology is to understand altruistic help and reproductive partitioning in cooperative societies, where subordinate helpers forego reproduction to rear dominant breeders' offspring. Traditional models of cooperation in these societies typically make a key assumption: that the only alternative to staying and helping is solitary breeding, an often unfeasible task. Using large-scale field experiments on paper wasps (Polistes dominula), we show that individuals have high-quality alternative nesting options available that offer fitness payoffs just as high as their actual chosen options, far exceeding payoffs from solitary breeding. Furthermore, joiners could not easily be replaced if they were removed experimentally, suggesting that it may be costly for dominants to reject them. Our results have implications for expected payoff distributions for cooperating individuals, and suggest that biological market theory, which incorporates partner choice and competition for partners, is necessary to understand helping behaviour in societies like that of P. dominula Traditional models are likely to overestimate the incentive to stay and help, and therefore the amount of help provided, and may underestimate the size of reproductive concession required to retain subordinates. These findings are relevant for a wide range of cooperative breeders where there is dispersal between social groups.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Using social parasitism to test reproductive skew models in a primitively eusocial wasp.

Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.

Dynamics of social queues.

Queues formed by social wasps to inherit the dominant position in the nest are analyzed by using a transient quasi-birth-and-death (QBD) process. We show that the extended nest lifespan due to division of labor between queen and helpers has a big impact on nest productivity.

Reduction of foraging work and cooperative breeding.

Using simple stochastic models, we discuss how cooperative breeders, especially wasps and bees, can improve their productivity by reducing foraging work. In a harsh environment, where foraging is the main cause of mortality, such breeders achieve greater productivity by reducing their foraging effort below full capacity, and they may thrive by adopting cooperative breeding. This could prevent the population extinction of cooperative breeders under conditions where a population of lone breeders cannot be maintained.

Genetic differentiation at extreme latitudes in the socially plastic sweat bee Halictus rubicundus.

The sweat bee Halictus rubicundus is an important pollinator with a large latitudinal range and many potential barriers to gene flow. Alongside typical physical barriers, including mountain ranges and oceans, the climate may also impose restrictions on gene flow in this species. The climate influences voltinism and sociality in H. rubicundus, which is bivoltine and can nest socially at warmer lower latitudes but tends to be univoltine and solitary in the cooler north. Variation in voltinism could result in phenological differences, potentially limiting gene flow, but a previous study found no evidence for this in H. rubicundus populations in mainland Britain. Here we extend the previous study to consider populations of H. rubicundus at extreme northern and southern latitudes in the UK. We found that bees from a population in the far north of Scotland were genetically differentiated from bees collected in Cornwall in the south-west of England. In contrast, bees collected across the Irish Sea in Northern Ireland showed slight genetic overlap with both the Scottish and Cornish bees. Our results suggest that when populations at extreme latitudes are considered, phenology and the climate may act alongside physical barriers such as the Scottish Highlands and the Irish Sea to restrict gene flow in H. rubicundus. We discuss the implications of our results for local adaptation in the face of rapidly changing selection pressures which are likely under climate change.

A cytochrome P450 insecticide detoxification mechanism is not conserved across the Megachilidae family of bees.

Recent work has demonstrated that many bee species have specific cytochrome P450 enzymes (P450s) that can efficiently detoxify certain insecticides. The presence of these P450s, belonging or closely related to the CYP9Q subfamily (CYP9Q-related), is generally well conserved across the diversity of bees. However, the alfalfa leafcutter bee, Megachile rotundata, lacks CYP9Q-related P450s and is 170-2500 times more sensitive to certain insecticides than bee pollinators with these P450s. The extent to which these findings apply to other Megachilidae bee species remains uncertain. To address this knowledge gap, we sequenced the transcriptomes of four Megachile species and leveraged the data obtained, in combination with publicly available genomic data, to investigate the evolution and function of P450s in the Megachilidae. Our analyses reveal that several Megachilidae species, belonging to the Lithurgini, Megachilini and Anthidini tribes, including all species of the Megachile genus investigated, lack CYP9Q-related genes. In place of these genes Megachile species have evolved phylogenetically distinct CYP9 genes, the CYP9DM lineage. Functional expression of these P450s from M. rotundata reveal they lack the capacity to metabolize the neonicotinoid insecticides thiacloprid and imidacloprid. In contrast, species from the Osmiini and Dioxyini tribes of Megachilidae have CYP9Q-related P450s belonging to the CYP9BU subfamily that are able to detoxify thiacloprid. These findings provide new insight into the evolution of P450s that act as key determinants of insecticide sensitivity in bees and have important applied implications for pesticide risk assessment.

Caste determination through mating in primitively eusocial societies.

Eusocial animal societies are typified by the presence of a helper (worker) caste which predominantly cares for young offspring in a social group while investing little in their own direct reproduction. A key question is what determines whether an individual becomes a worker or leaves to initiate her own reproduction. In some insects, caste is determined nutritionally during development. In others, and in vertebrate societies, adults are totipotent and the cues that determine caste are less well known. The mate limitation hypothesis (MLH) states that a female's mating status acts as a cue for caste determination: females that mate become reproductives, while those that fail to mate become workers. The MLH is consistent with empirical observations in sweat bees showing that over the course of the nesting season, there are increases in both the proportion of females that become reproductives and the frequency of males in the mating pool. We modelled a foundress's offspring sex-ratio strategy to investigate whether an increasingly male-biased operational sex-ratio over time is evolutionarily stable under the MLH. Our results indicate that such a pattern could occur if early workers were more valuable than late workers. This pattern was then more likely if male mortality was high, if worker mortality was low, if the value of a worker was high and if the period over which workers can help was short. Our results suggest that the MLH can be evolutionarily stable, but only under restrictive conditions. Manipulative experiments are now required to investigate whether mating determines caste in nature.

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects.

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.

Future fitness and helping in social queues.

Helpers in primitively eusocial and cooperatively breeding animal societies forfeit their own reproduction to rear the offspring of a queen or breeding pair, but may eventually attain breeding status themselves. Kin selection provides a widely accepted theoretical framework for understanding these societies, but differences in genetic relatedness do not explain a universal societal feature: the huge variation between individuals in helping effort. An alternative explanation for this variation lies in a fundamental trade-off faced by helpers: by working harder, they increase the indirect component of their fitness, but simultaneously decrease their own future survival and fecundity. Here, we show that individuals work less hard when they stand to lose more future fitness through working. We experimentally manipulated two components of future fitness in social queues of hover wasps (Stenogastrinae): a helper's chance of inheriting an egg-laying position, and the workforce available to rear her offspring should she inherit. After each manipulation, helpers increased or decreased their effort as appropriate to the change in expected future fitness that they experienced. Although helping provides significant indirect fitness benefits for hover wasps, our study shows that variation in the costs associated with helping is the major determinant of helping effort.

Male survivorship and the evolution of eusociality in partially bivoltine sweat bees.

Eusociality, where workers typically forfeit their own reproduction to assist their mothers in raising siblings, is a fundamental paradox in evolutionary biology. By sacrificing personal reproduction, helpers pay a significant cost, which must be outweighed by indirect fitness benefits of helping to raise siblings. In 1983, Jon Seger developed a model showing how in the haplodiploid Hymenoptera (ants, wasps and bees), a partially bivoltine life cycle with alternating sex ratios may have promoted the evolution of eusociality. Seger predicted that eusociality would be more likely to evolve in hymenopterans where a foundress produces a male-biased first brood sex ratio and a female-biased second brood. This allows first brood females to capitalize on super-sister relatedness through helping to produce the female-biased second brood. In Seger's model, the key factor driving alternating sex ratios was that first brood males survive to mate with females of both the second and the first brood, reducing the reproductive value of second brood males. Despite being potentially critical in the evolution of eusociality, however, male survivorship has received little empirical attention. Here, we tested whether first brood males survive across broods in the facultatively eusocial sweat bee Halictus rubicundus. We obtained high estimates of survival and, while recapture rates were low, at least 10% of first brood males survived until the second brood. We provide empirical evidence supporting Seger's model. Further work, measuring brood sex ratios and comparing abilities of first and second brood males to compete for fertilizations, is required to fully parameterize the model.

Assured fitness returns in a social wasp with no worker caste.

The theory of assured fitness returns proposes that individuals nesting in groups gain fitness benefits from effort expended in brood-rearing, even if they die before the young that they have raised reach independence. These benefits, however, require that surviving nest-mates take up the task of rearing these young. It has been suggested that assured fitness returns could have favoured group nesting even at the origin of sociality (that is, in species without a dedicated worker caste). We show that experimentally orphaned brood of the apoid wasp Microstigmus nigrophthalmus continue to be provisioned by surviving adults for at least two weeks after the orphaning. This was the case for brood of both sexes. There was no evidence that naturally orphaned offspring received less food than those that still had mothers in the nest. Assured fitness returns can therefore represent a real benefit to nesting in groups, even in species without a dedicated worker caste.

Simple trapeziectomy versus trapeziectomy with flexor carpi radialis suspension: a 17-year follow-up of a randomized blind trial.

The purpose of this study was to investigate if there were any significant differences in the long-term outcomes of patients who participated in a randomized trial of trapeziectomy alone compared with trapeziectomy with ligament reconstruction and tendon interposition (LRTI). Sixty-five patients were invited for a follow-up visit at a mean of 17 years (range 15-20) postoperatively. Twenty-eight patients attended, who had 34 operations, 14 trapeziectomy alone and 20 with LRTI. There were no statistically significant differences between the two groups in terms of satisfaction with surgery or functional outcomes, with most measurements showing minimal or no differences in means between the two groups. There was no difference in the space between the metacarpal and scaphoid. Radial abduction was the only parameter that was significantly greater in the patients with simple trapeziectomy (median 79°) compared with trapeziectomy with LRTI (median 71°) (p = 0.04). Even at 17 years there is no significant benefit of LRTI over trapeziectomy alone for thumb carpometacarpal joint osteoarthritis.Level of evidence: I.

Massive transfusion experience, current practice and decision support: A survey of Australian and New Zealand anaesthetists.

Massive transfusions guided by massive transfusion protocols are commonly used to manage critical bleeding, when the patient is at significant risk of morbidity and mortality, and multiple timely decisions must be made by clinicians. Clinical decision support systems are increasingly used to provide patient-specific recommendations by comparing patient information to a knowledge base, and have been shown to improve patient outcomes. To investigate current massive transfusion practice and the experiences and attitudes of anaesthetists towards massive transfusion and clinical decision support systems, we anonymously surveyed 1000 anaesthetists and anaesthesia trainees across Australia and New Zealand. A total of 228 surveys (23.6%) were successfully completed and 227 were analysed for a 23.3% response rate. Most respondents were involved in massive transfusions infrequently (88.1% managed five or fewer massive transfusion protocols per year) and worked at hospitals which have massive transfusion protocols (89.4%). Massive transfusion management was predominantly limited by timely access to point-of-care coagulation assessment and by competition with other tasks, with trainees reporting more significant limitations compared to specialists. The majority of respondents reported that they were likely, or very likely, both to use (73.1%) and to trust (85%) a clinical decision support system for massive transfusions, with no significant difference between anaesthesia trainees and specialists (P = 0.375 and P = 0.73, respectively). While the response rate to our survey was poor, there was still a wide range of massive transfusion experience among respondents, with multiple subjective factors identified limiting massive transfusion practice. We identified several potential design features and barriers to implementation to assist with the future development of a clinical decision support system for massive transfusion, and overall wide support for a clinical decision support system for massive transfusion among respondents.