Solitary Ancestors Research Articles

Costs of reproduction are present but latent in eusocial bumblebee queens

BackgroundThe standard evolutionary theory of ageing proposes that ageing occurs because of a trade-off between reproduction and longevity. Eusocial insect queens exhibit positive fecundity-longevity associations and so have been suggested to be counter-examples through not expressing costs of reproduction and through remodelling conserved genetic and endocrine networks regulating ageing and reproduction. If so, eusocial evolution from solitary ancestors with negative fecundity-longevity associations must have involved a stage at which costs of reproduction were suppressed and fecundity and longevity became positively associated. Using the bumblebee (Bombus terrestris), we experimentally tested whether queens in annual eusocial insects at an intermediate level of eusocial complexity experience costs of reproduction, and, using mRNA-seq, the extent to which they exhibit a remodelling of relevant genetic and endocrine networks. Specifically, we tested whether costs of reproduction are present but latent, or whether a remodelling of relevant genetic and endocrine networks has already occurred allowing queens to reproduce without costs.ResultsWe experimentally increased queens’ costs of reproduction by removing their eggs, which caused queens to increase their egg-laying rate. Treatment queens had significantly reduced longevity relative to control queens whose egg-laying rate was not increased. Reduced longevity in treatment queens was not caused by increased worker-to-queen aggression or by increased overall activity in queens. In addition, treatment and control queens differed in age-related gene expression based on mRNA-seq in both their overall expression profiles and the expression of ageing-related genes. Remarkably, these differences appeared to occur principally with respect to relative age, not chronological age.ConclusionsThis study represents the first simultaneously phenotypic and transcriptomic experimental test for a longevity cost of reproduction in eusocial insect queens. The results support the occurrence of costs of reproduction in annual eusocial insects of intermediate social complexity and suggest that reproductive costs are present but latent in queens of such species, i.e. that these queens exhibit condition-dependent positive fecundity-longevity associations. They also raise the possibility that a partial remodelling of genetic and endocrine networks underpinning ageing may have occurred in intermediately eusocial species such that, in unmanipulated conditions, age-related gene expression depends more on chronological than relative age.

A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism

Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.

Social divergence: molecular pathways underlying castes and longevity in a facultatively eusocial small carpenter bee.

Unravelling the evolutionary origins of eusocial life is a longstanding endeavour in the field of evolutionary-developmental biology. Descended from solitary ancestors, eusocial insects such as honeybees have evolved ontogenetic division of labour in which short-lived workers perform age-associated tasks, while a long-lived queen produces brood. It is hypothesized that (i) eusocial caste systems evolved through the co-option of deeply conserved genes and (ii) longevity may be tied to oxidative damage mitigation capacity. To date, however, these hypotheses have been examined primarily among only obligately eusocial corbiculate bees. We present brain transcriptomic data from a Japanese small carpenter bee, Ceratina japonica (Apidae: Xylocopinae), which demonstrates both solitary and eusocial nesting in sympatry and lives 2 or more years in the wild. Our dataset captures gene expression patterns underlying first- and second-year solitary females, queens and workers, providing an unprecedented opportunity to explore the molecular mechanisms underlying caste-antecedent phenotypes in a long-lived and facultatively eusocial bee. We find that C. japonica's queens and workers are underpinned by divergent gene regulatory pathways, involving many differentially expressed genes well-conserved among other primitively eusocial bee lineages. We also find support for oxidative damage reduction as a proximate mechanism of longevity in C. japonica.

What Can Mechanisms Underlying Derived Traits Tell Us About the Evolution of Social Behavior?

AbstractSocial behavior, although rare, is a highly successful form of living that has reached its most extreme forms in eusocial insects. A tractable framework to understand social evolution is the study of major transitions in social behavior. This includes the transitions between solitary to social living, from species exhibiting intermediate degrees of sociality to species exhibiting true sociality, and from primitive to advanced eusocial species. The latter transition is characterized by the emergence of traits not previously found in primitive eusocial species, such as fixed morphological differences between castes and task specialization within the sterile caste. Such derived traits appear to exist in a binary fashion, present in advanced eusocial species, and absent or rare in primitive ones, and thus do not exist in a gradient that is easily tracked and compared between species. Thus, they may not be viewed as valuable to explore ultimate questions related to social evolution. Here, we argue that derived traits can provide useful insights on social evolution even if they are absent or rare in species with a lower social organization. This applies only if the mechanism underlying the trait, rather than the function it regulates for, can be traced back to the solitary ancestors. We discuss two examples of derived traits, morphological differences in female castes and primer pheromones regulating female reproduction, demonstrating how their underlying mechanisms can be used to understand major transitions in the evolution of social behavior and emphasize the importance of studying mechanistic, rather than functional continuity of traits.

An ecological driver for the macroevolution of morphological polymorphism within colonial invertebrates.

Colonial marine invertebrates, such as corals and bryozoans, have modular growth. Individual modules within a colony are homologous to an individual solitary animal body. But in contrast to the predominately sexual origin of solitary animal bodies, modules within a colony are always produced asexually. The repetition of modules and the indeterminism of their organization gives colonies the ability to grow in ways solitary animals cannot. Colonial invertebrates consequently grow in such a way as to resemble weeds, bushes, or trees. The multitude of growth forms of colonial invertebrates arise from differences how individual colonies within a species tend to invest their energy into modular growth, persistence, asexual propagation, and sexual reproduction. Moreover, many colonial invertebrates possess several body types, morphological polymorphism among modules, where modules qualitatively differ in shape, size, and function. In this paper, I propose a mechanism that links the origin of novel body types to the evolution of life‐history strategies among species. When colonies first evolve from solitary ancestors, the life‐history strategy of the colony remains constrained by the life‐history strategies of the individual modules within the colony until a new polymorph type evolves. The addition of novel body types within a colony introduces potential variation in life‐history strategies. Colonies can then change strategies by regulating the frequencies of body types within the colony. This, along with the ability of body types to simplify their structure permits colonies to evolve more complex life‐histories. Each new polymorph type that evolves permits more variation in colonial life‐histories to exist.

Mating status and the evolution of eusociality: Oogenesis is independent of mating status in the solitary bee Osmia bicornis

The fundamental trait underlying eusociality is the reproductive division of labour. In honeybees (Apis mellifera), queens lay eggs while workers forage, defend and care for brood. The division of labour is maintained by pheromones including queen mandibular pheromone (QMP) produced by the queen. QMP constrains reproduction in adult honeybee workers, but in the absence of their queen workers can activate their ovaries and, although they cannot mate, they lay haploid male eggs. The reproductive ground plan hypothesis suggests that reproductive constraint may have evolved by co-opting mechanisms of reproductive control in solitary ancestors. In many insects mating is required to activate or accelerate oogenesis. Here, we use the solitary bee Osmia bicornis (Megachilidae) to test whether reproductive constraint evolved from ancestral control of reproduction by mating status. We present a structural study of the O. bicornis ovary, and compare key stages of oogenesis with honeybee workers. Importantly, we show that mating does not affect any aspect of the reproductive physiology of O. bicornis. We therefore conclude that mechanisms governing reproductive constraint in honeybees were unlikely to have been co-opted from mechanisms pertaining to mating status.

Evolutionary transitions toward pair living in nonhuman primates as stepping stones toward more complex societies.

Nonhuman primate societies vary tremendously in size and composition, but how and why evolutionary transitions among different states occurred remains highly controversial. In particular, how many times pair living evolved and the social states of the ancestors of pair- and group-living species remains contentious. We examined evolutionary transitions in primate social evolution by using new, independent categorizations of sociality and different phylogenetic hypotheses with a vastly expanded dataset. Using Bayesian phylogenetic comparative methods, we consistently found the strongest support for a model that invokes frequent transitions between solitary ancestors and pair-living descendants, with the latter giving rise to group-living species. This result was robust to systematic variation in social classification, sample size, and phylogeny. Our analyses therefore indicate that pair living was a stepping stone in the evolution of structurally more complex primate societies, a result that bolsters the role of kin selection in social evolution.

Social modularity: conserved genes and regulatory elements underlie caste-antecedent behavioural states in an incipiently social bee.

The evolutionary origins of advanced eusociality, one of the most complex forms of phenotypic plasticity in nature, have long been a focus within the field of sociobiology. Although eusocial insects are known to have evolved from solitary ancestors, sociogenomic research among incipiently social taxa has only recently provided empirical evidence supporting theories that modular regulation and deeply conserved genes may play important roles in both the evolutionary emergence and elaboration of insect sociality. There remains, however, a paucity of data to further test the biological reality of these and other evolutionary theories among taxa in the earliest stages of social evolution. Here, we present brain transcriptomic data from the incipiently social small carpenter bee, Ceratina calcarata, which captures patterns of cis-regulation and gene expression associated with female maturation, and underlying two well-defined behavioural states, foraging and guarding, concurrently demonstrated by mothers and daughters during early autumn. We find that an incipiently social nest environment may dramatically affect gene expression. We further reveal foraging and guarding behaviours to be putatively caste-antecedent states in C. calcarata, and offer strong empirical support for the operation of modular regulation, involving deeply conserved and differentially expressed genes in the expression of early social forms.

Catalyzing Transitions to Sociality: Ecology Builds on Parental Care

In the context of social evolution research, a great emphasis on kin-selected benefits has led to understand parental care as one of the activities that helpers can perform in extended cooperative families. Nevertheless, this perspective might have precluded a deeper understanding of the implications of parental care for social evolution. We argue that parental care is a broader set of processes playing a key role both before and during the emergence of sociality. The care system of a species may be understood as the result of long coevolutionary processes with environmental pressures during pre-social stages that impact transitions to sociality. We evaluate the present framework against evidence on the evolution of parental care and transitions towards sociality in subsocial and parasocial vertebrate and invertebrate species. Moreover, following previous evidence for the importance of modes of foraging and resting we structure our inquiry by classifying societies into three types. Our results suggest that in central place foragers and fortress defenders, ecological factors promoting the evolution of parental care foster a set of coevolutionary feedback loops resulting in increases in parental effort and offspring needs. Offspring needs alone or in combination with limited breeding options enhance the relative benefits of positive social interactions, catalyzing social transitions. In itinerant foragers, sociality is associated with colonizing new niches. Changes in predation pressure entail changes in the modes of care or selection for certain types of care present already in solitary ancestors. Further changes in the form of collective defense may be needed for permanent sociality to evolve. We conclude there is evidence that social transitions to different types of societies are the result of long coevolutionary processes between environmental pressures and the care systems in a wide variety of taxa. Therefore, advances in the study of the origins of sociality may need from further investigation of parental care evolution in solitary ancestors of today's social species.

Synthesis of Tinbergen’s four questions and the future of sociogenomics

It has been 55 years since Nikolaas Tinbergen formalized the field of ethology by identifying four types of inquiry that address the “how” and “why” of animal behavior from both a contemporary and historical perspective. This framework has been particularly useful in exploring eusocial behavior among insects, due to integration across levels of analysis and timescales of influence. Although the former has proceeded quite deliberately, the latter has received less attention. Here, I synthesize recent findings regarding the mechanisms, ontogeny, evolution, and function of eusociality in ants, bees, and wasps. This synthesis reveals that there has been rapid gain of knowledge regarding the genetic underpinnings of eusocial behavior, but an understanding of the fitness consequences of these molecular mechanisms lags behind. Similarly, it has become clear that maternal or sibling effects on development are major drivers of caste-related behavior, but the mechanisms that produce these effects are largely unknown. Developmental caste determination and caste-biasing require sensitivities to social cues, but how this plasticity evolved from solitary ancestors is unknown. Understanding the origins of developmental plasticity is necessary to understand how plasticity shapes the evolutionary trajectory of social traits. Likewise, the influence of social function on molecular evolution has been studied within a robust theoretical framework; however, these studies will benefit from an understanding of how ancestral conditions promote the acquisition of social function in the first place. Future studies that span both levels of analysis and timescales of influence will further advance the integrative field of ethology that Tinbergen envisioned.

Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia

BackgroundGlycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In multicellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like differentiation. We investigated whether, similar to other sporulation-inducing genes such as cAMP-dependent protein kinase (PKA), this role of GSK3 is derived from an ancestral role in encystation of unicellular amoebas.ResultsWe deleted GSK3 in Polysphondylium pallidum, a group 2 dictyostelid which has retained encystation as an alternative survival strategy. Loss of GSK3 inhibited cytokinesis of cells in suspension, as also occurs in D. discoideum, but did not affect spore or stalk differentiation in P. pallidum. However, gsk3− amoebas entered into encystation under conditions that in wild type favour aggregation and fruiting body formation. The gsk3− cells were hypersensitive to osmolytes, which are known to promote encystation, and to cyst-inducing factors that are secreted during starvation. GSK3 was not itself regulated by these factors, but inhibited their effects.ConclusionsOur data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore differentiation in Dictyostelia. Instead, in P. pallidum, one of many Dictyostelia that like their solitary ancestors can still encyst to survive starvation, GSK3 promotes multicellular development into fruiting bodies over unicellular encystment.

TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.

A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.

Primer effects of the honeybee, Apis mellifera, queen pheromone 9-ODA on drones

In many social insect species, pheromones coordinate defining features of social life. Queen-produced pheromones mediate many of these processes, and thus there is substantial interest in understanding both the mechanisms by which queen pheromones organize behaviour and how these chemical communication systems evolved. It is hypothesized that queen social pheromones evolved from sex pheromones found in their solitary ancestors. Here we begin to test this theory in the honeybee, where the queen-produced pheromone 9-ODA (9-oxo-2-decenoic acid) serves as both a social pheromone (priming physiological processes mediating worker behavioural maturation) and sex pheromone (attracting males during mating flights). While we expected the primer effects of 9-ODA on workers to represent a derived worker-specific function, we surprisingly found similar effects in drones. Exposure to 9-ODA resulted in a significant increase in expression levels of vitellogenin in drones. Since previous studies in workers found that vitellogenin levels regulate behavioural maturation, we investigated 9-ODA's effects on sexual maturation in drones. Drones exposed to 9-ODA initiated mating flights later and took fewer flights than control drones. Our results demonstrate that honeybee queen pheromone has primer effects on drone bees, and thus chemical communication systems involving honeybee drones are more complex than previously appreciated.

Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris.

Understanding the social evolution leading to insect eusociality requires, among other, a detailed insight into endocrine regulatory mechanisms that have been co-opted from solitary ancestors to play new roles in the complex life histories of eusocial species. Bumblebees represent well-suited models of a relatively primitive social organization standing on the mid-way to highly advanced eusociality and their queens undergo both, a solitary and a social phase, separated by winter diapause. In the present paper, we characterize the gene expression levels of major endocrine regulatory pathways across tissues, sexes, and life-stages of the buff-tailed bumblebee, Bombus terrestris, with special emphasis on critical stages of the queen's transition from solitary to social life. We focused on fundamental genes of three pathways: (1) Forkhead box protein O and insulin/insulin-like signaling, (2) Juvenile hormone (JH) signaling, and (3) Adipokinetic hormone signaling. Virgin queens were distinguished by higher expression of forkhead box protein O and downregulated insulin-like peptides and JH signaling, indicated by low expression of methyl farnesoate epoxidase (MFE) and transcription factor Krüppel homolog 1 (Kr-h1). Diapausing queens showed the expected downregulation of JH signaling in terms of low MFE and vitellogenin (Vg) expressions, but an unexpectedly high expression of Kr-h1. By contrast, reproducing queens revealed an upregulation of MFE and Vg together with insulin signaling. Surprisingly, the insulin growth factor 1 (IGF-1) turned out to be a queen-specific hormone. Workers exhibited an expression pattern of MFE and Vg similar to that of reproducing queens. Males were characterized by high Kr-h1 expression and low Vg level. The tissue comparison unveiled an unexpected resemblance between the fat body and hypopharyngeal glands across all investigated genes, sexes, and life stages.

Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae).

The evolution of complex societies with obligate reproductive division of labor represents one of the major transitions in evolution. In such societies, functionally sterile individuals (workers) perform many of fitness-relevant behaviors including allomaternal ones, without getting any direct fitness benefits. The question of how such worker division of labor has evolved remains controversial. The reproductive groundplan hypothesis (RGPH) offers a powerful proximate explanation for this evolutionary leap. The RGPH argues that the conserved genetic and endocrinological networks regulating fitness-relevant behavior (e g. foraging and brood care) in their solitary ancestors have become decoupled from actual reproduction in the worker caste and now generate worker behavioral phenotypes. However, the empirical support for this hypothesis remains limited to a handful of species making its general validity uncertain. In this study, we combine data from the literature with targeted sampling of key species and apply phylogenetically controlled comparative analysis to investigate if the key prediction of the RGPH, namely an association between allomaternal behavior and an allomaternal physiological state holds in the largest and most species-rich clade of social insects, the ants. Our findings clearly support the RPGH as a general framework to understand the evolution of the worker caste and shed light on one of the major transition in evolutionary history.

ДЕЦЕНТРАЛИЗОВАННЫЙ ОРГАНИЗМ НА ПРИМЕРЕ КОЛОНИАЛЬНЫХ ГИДРОИДОВ

Колониальные гидроиды, кораллы, мшанки, асцидии и некоторые другие водные организмы состоят как будто из множества соединенных друг с другом особей. Но это – не сообщества особей, а многочленные особи, приспособленные к перехвату пищевых частиц из потока воды, с чем, видимо, связано сходство колониальных животных с растениями, которые приспособлены к эффективному перехвату солнечного света. Считается, что у животных колониальная организация возникла в результате незавершенного вегетативного размножения, когда молодые особи остаются связанными с материнской особью. Многочленный (или модульный) организм оказывается менее целостным и централизованным, чем его одиночный (унитарный) предок. Строение децентрализованного организма позволяет изучать интеграцию частей в целое, реализованную без участия органов управления. Такое соотношение частей и целого свойственно многим природным и социальным системам, но до сих пор мало изучено. Особые органы управления (нервная и гуморальная системы) лишь надстроены над более простым типом взаимного согласования процессов, который является единственным у децентрализованных организмов, где интеграция основана на множественном взаимодействии относительно независимых паритетных частей целого. Среди различных видов децентрализованных организмов наиболее удобны для исследований колониальные гидроиды, которые могут быть биологической моделью нецентрализованной системы как таковой. Децентрализованная организация у колониальных гидроидов выражается в следующем: 1) мультипликация (или полимеризация); 2) отсутствие общеорганизменных регуляторных органов; 3) значительная самостоятельность составляющих; 4) высокая устойчивость к воздействиям на отдельные части организма; 5) пластичность формы и широкая вариативность размеров взрослого организма; 6) «врастание» в окружающую среду; 7) сетевидная форма организма; 8) циклический морфогенез; 9) преодоление возрастных ограничений. Обсуждены характерные особенности децентрализованных организмов и возможности экстраполяции полученных выводов на надорганизменные системы: популяции, экосистемы, биосферу.

The origin and evolution of queen and fertility signals in Corbiculate bees.

BackgroundIn social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors.ResultsHere, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species.ConclusionOverall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0509-8) contains supplementary material, which is available to authorized users.

The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems.

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against their own best interests.

Cheating workers with large activated ovaries avoid risky foraging

Eusocial insects undoubtedly evolved from solitary ancestors, but how this occurred is not well established. The Ground Plan hypothesis suggests that gene networks that once regulated the oviposition and foraging phases of an ancestral solitary insect’s life cycle have been co-opted to establish the queen–worker dimorphism in extant eusocial insects; queens permanently express genes that were once expressed during the oviposition phase, whereas workers express genes that were once associated with foraging. An extension of the Ground Plan hypothesis, the Reproductive Ground Plan-forager hypothesis, proposes that foraging specialization by worker honey bees for either pollen or nectar is controlled by the same reproductive gene networks. According to the Reproductive Ground Plan-forager hypothesis, workers with more ovarioles forage early in life and specialize in pollen collection. Here we find that among workers of a highly reproductive honey bee subspecies, Apis mellifera capensis, there is a positive correlation between ovariole number and age at onset of foraging, and no association between ovariole number and foraging preference, thus contradicting key aspects of the Reproductive Ground Plan-forager hypothesis. We also find a negative association between ovariole number and ovary activation, suggesting that high ovariole number is not directly related to reproductive potential as previously assumed.

Worker division of labor and endocrine physiology are associated in the harvester ant,Pogonomyrmex californicus

In Pogonomyrmex californicus harvester ants, an age-associated division of labor occurs in the worker caste, in which young workers perform in-nest tasks and older workers forage for food. Here, we tested whether this behavioral division is age based or age flexible, and whether it coincides with differential expression of systemic hormones with known roles in behavioral regulation. Whole-body content of juvenile hormone (JH) and ecdysteroids was determined in workers from (1) age-typical colonies, in which a typical age structure is maintained and workers transition across behaviors naturally, and (2) single-cohort colonies, which are entirely composed of same-aged workers, facilitating the establishment of age-independent division of labor. Foragers from both colony types had higher JH and lower ecdysteroid content than workers performing in-nest tasks, suggesting that age is not the sole determinant of worker behavior. This association between hormone content and behavior of P. californicus workers is similar to that previously observed in founding queens of this species. Because these hormones are key regulators of development and reproductive behavior, our data are consistent with the reproductive ground plan hypothesis (RGPH), which posits that the reproductive regulatory mechanisms of solitary ancestors were co-opted to regulate worker behavior.