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Caste-biased gene expression in a facultatively eusocial bee suggests a role for genetic accommodation in the evolution of eusociality

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Abstract

Developmental plasticity may accelerate the evolution of phenotypic novelty through genetic accommodation, but studies of genetic accommodation often lack knowledge of the ancestral state to place selected traits in an evolutionary context. A promising approach for assessing genetic accommodation involves using a comparative framework to ask whether ancestral plasticity is related to the evolution of a particular trait. Bees are an excellent group for such comparisons because caste-based societies (eusociality) have evolved multiple times independently and extant species exhibit different modes of eusociality. We measured brain and abdominal gene expression in a facultatively eusocial bee, Megalopta genalis, and assessed whether plasticity in this species is functionally linked to eusocial traits in other bee lineages. Caste-biased abdominal genes in M. genalis overlapped significantly with caste-biased genes in obligately eusocial bees. Moreover, caste-biased genes in M. genalis overlapped significantly with genes shown to be rapidly evolving in multiple studies of 10 bee species, particularly for genes in the glycolysis pathway and other genes involved in metabolism. These results provide support for the idea that eusociality can evolve via genetic accommodation, with plasticity in facultatively eusocial species like M. genalis providing a substrate for selection during the evolution of caste in obligately eusocial lineages. © 2017 The Author(s) Published by the Royal Society. All rights reserved.

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... For instance, recent works have indicated that similar behavioural states and reproductive roles among independent social bee lineages may be underpinned by consistent differential expression of deeply conserved genes [25][26][27]. Research has also revealed that worker-like roles often feature expanded regulatory elements and evidence of positive protein evolution [28,29], as predicted by genetic release (in which otherwise pleiotropically constrained genes may be available for co-option into novel roles) [30]. Gene co-option and positive selection are expected to lead to the development of increasingly novel (taxonomically restricted) genes during further evolutionary derivations of social traits (e.g. ...
... Rank-rank hypergeometric overlap (RRHO) analyses of gene expression variation [53] between queens and workers of C. japonica and comparable roles in eight additional hymenopteran species (C. australensis [25]; M. genalis [28]; C. calcarata [29]; E. robusta; E. tridentata [34]; A. mellifera [54]; T. longispinosus [55]; and Polistes metricus [56]) collectively identified a total of 3328 genes significantly correlated in all comparisons to bees and a paper wasp ( p < 0.0001; figure 5; electronic supplementary material, table S17). Notably, this list of genes included a handful found to be significantly differentially expressed in both this study and others via BLASTn and OrthoFinder v 2.3.2 [57] (figure 6; electronic supplementary material, tables S18-S20). ...
... By far, the strongest correlations in gene expression were detected between C. japonica and other Ceratina species (i.e. C. calcarata [29] and C. australensis [25]) and between C. japonica and other primitive eusocial bees (M. genalis [28] and E. robusta [34]). ...
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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 ontogen-etic 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 transcrip-tomic 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.
... The crepuscular sweat bee (M. genalis ), for instance, nests either solitarily or in small, primitively eusocial colonies (Smith et al. 2003;Wcislo et al. 2004;Kapheim et al. 2013;Jones et al. 2017). The subsocial small carpenter bee (C. ...
... The abdominal gene expression patterns of workers that became replacement queens mirrored those of reproductive foundresses, while those of non-reproductive worker daughters stood apart. Differences in brain gene expression patterns among castes were not nearly as strong, however, suggesting that changes in reproductive functionality may precede changes in behavior (Jones et al. 2017). The caste-biased differences in abdominal gene expression detected in M. genalis were found to overlap with those of obligately eusocial taxa, suggesting there may be considerable conservation of the regulatory mechanisms underlying eusocial organization across evolutionary lineages. ...
... Recent sociogenomic research in M. genalis , however, offers the first empirical assessment of this idea in a facultatively eusocial species (Jones et al. 2017). Jones et al. (2017) found that genes with worker-biased expression in M. genalis overlapped with genes shown to be rapidly evolving in ten other bee species. ...
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Facultatively social species exhibit behavioral plasticity in response to changes in ecological conditions and social environment, and thus provide a natural experiment to compare solitary and social behaviors in a single genome. Such species can therefore provide empirical insights into the evolution of eusociality. The small carpenter bees (genus Ceratina) and sweat bees (Halictidae) are of special interest because they exhibit rich behavioral plasticity. Species range from solitary to eusocial, and both groups benefit from detailed behavioral research and well-established phylogenies. As such, small carpenter and sweat bees are poised to further comparative sociogenomic studies which emphasize the necessity of a molecular phylogeny for understanding the evolution of molecular architecture underlying social phenotypes and organizational complexity. Here, we review behavioral, transcriptomic and genomic data in bees across the social spectrum, highlighting the importance of simple societies and facultatively social taxa to examine the genetic basis of cooperative traits and social evolution.
... Indeed, few examples of genetic accommodation have been elucidated to this level in the laboratory or in natural populations (e.g. Casasa and Moczek, 2018;Dworkin, 2005;Jones et al., 2017;Suzuki and Nijhout, 2006;reviewed in Renn and Schumer, 2013;Schlichting and Wund, 2014). However, it is unclear whether the current low number of genetic accommodation examples reflects actual rarity in nature, or a combination of low research effort together with a lack of known mechanisms. ...
... Criterion 1: the focal trait can be environmentally induced in ancestral-proxy lineages Reproductive division of labor has been induced experimentally in multiple solitary and subsocial species through forced association studies, where typically non-associating females are forced to cohabit. Many examples come from the small carpenter bees (Sakagami and Maeta, 1984 and sweat bees (Jeanson et al., 2005(Jeanson et al., , 2008, groups that show high levels of social plasticity and may be especially useful for assessing genetic accommodation (Jones et al., 2017;Kocher and Paxton, 2014;Shell and Rehan, 2017). In some cases, a single species displays both solitary and social forms (Davison and Field, 2016;Smith et al., 2003;Soucy and Danforth, 2002), and in situations where these forms are Maeta, 1984, 1987), Ceratina okinawana (Sakagami and Maeta, 1989), Lasioglossum spp. ...
... Other work has successfully manipulated the social environment (Robinson et al., 1989(Robinson et al., , 1992Ross and Keller, 2002), including changing colony demographics in 'pseudomutant' colonies and comparing the performance of this artificial construct with naturally formed colonies (Wilson, 1985), as well as many instances of queen removals to induce worker reproduction across ants, bees and wasps (e.g. Dietemann and Peeters, 2000;Jones et al., 2017;Reeve and Gamboa, 1987). What is unique about the eusocial engineering approach is the coupling of these manipulative studies with artificial selection and multiple genetic, transcriptomic and epigenetic monitoring approaches, enabling real-time tracking of the plastic and heritable components of environmentally induced traits. ...
Article
For over a century, biologists have proposed a role for phenotypic plasticity in evolution, providing an avenue for adaptation in addition to 'mutation-first' models of evolutionary change. According to the various versions of this idea, the ability of organisms to respond adaptively to their environment through phenotypic plasticity may lead to novel phenotypes that can be screened by natural selection. If these initially environmentally induced phenotypes increase fitness, then genetic accommodation can lead to allele frequency change, influencing the expression of those phenotypes. Despite the long history of 'plasticity-first' models, the importance of genetic accommodation in shaping evolutionary change has remained controversial - it is neither fully embraced nor completely discarded by most evolutionary biologists. We suggest that the lack of acceptance of genetic accommodation in some cases is related to a lack of information on its molecular mechanisms. However, recent reports of epigenetic transgenerational inheritance now provide a plausible mechanism through which genetic accommodation may act, and we review this research here. We also discuss current evidence supporting a role for genetic accommodation in the evolution of eusociality in social insects, which have long been models for studying the influence of the environment on phenotypic variation, and may be particularly good models for testing hypotheses related to genetic accommodation. Finally, we introduce 'eusocial engineering', a method by which novel social phenotypes are first induced by environmental modification and then studied mechanistically to understand how environmentally induced plasticity may lead to heritable changes in social behavior. We believe the time is right to incorporate genetic accommodation into models of the evolution of complex traits, armed with new molecular tools and a better understanding of non-genetic heritable elements.
... parental care have reveal interesting and unexpected results, such as the frequent losses as well as gains reconstructed for eusociality (Wcislo and Danforth 1997;Schwarz et al. 2003). Combining inferences from phylogenetic work with empirical studies also suggests that the the diversity of social systems seen in the Hymenoptera may stem from plasticity in facultatively eusocial ancestors (Jones et al. 2017). ...
... The 'flexible stem hypothesis' suggests that plasticity in an ancestral lineage can result in replicate descendant lineages in which one of the once environmentally induced phenotypes has become fixed ('genetic assimilation';West-Eberhard 2003;Wund et al. 2008). A similar process has been suggested to occur during evolutionary pathways to eusociality, where phenotypic plasticity exhibited by facultatively eusocial species is the substrate for selection (Jones et al. 2017). When selection is consistent, traits are thought to become canalised, environmental sensitivity is lost and obligate eusociality and caste dimorphism arise (Jones et al. 2017). ...
... A similar process has been suggested to occur during evolutionary pathways to eusociality, where phenotypic plasticity exhibited by facultatively eusocial species is the substrate for selection (Jones et al. 2017). When selection is consistent, traits are thought to become canalised, environmental sensitivity is lost and obligate eusociality and caste dimorphism arise (Jones et al. 2017). ...
Article
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Insect parental care strategies are particularly diverse, and prolonged association between parents and offspring may be a key precursor to the evolution of complex social traits. Macroevolutionary patterns remain obscure, however, due to the few rigorous phylogenetic analyses. The subsocial sphecid wasps are a useful group in which to study parental care because of the diverse range of strategies they exhibit. These strategies range from placing a single prey item in a pre-existing cavity to mass provisioning a pre-built nest, through to complex progressive provisioning where a female feeds larvae in different nests simultaneously as they grow. We show that this diversity stems from multiple independent transitions between states. The strategies we focus on were previously thought of in terms of a stepping-stone model in which complexity increases during evolution, ending with progressive provisioning which is a likely precursor to eusociality. We find that evolution has not always followed this model: reverse transitions are common, and the ancestral state is the most flexible rather than the simplest strategy. Progressive provisioning has evolved several times independently, but transitions away from it appear rare. We discuss the possibility that ancestral plasticity has played a role in the evolution of extended parental care. Significance statement Parental care behaviour leads to prolonged associations between parents and offspring, which is thought to drive the evolution of social living. Despite the importance of insect parental care for shaping the evolution of sociality, relatively few studies have attempted to reconstruct how different strategies evolve in the insects. In this study, we use phylogenetic methods to reconstruct the evolution of the diverse parental care strategies exhibited by the subsocial digger wasps (Sphecidae). Contrary to expectations, we show that parental care in this group has not increased in complexity over evolutionary time. We find that the ancestral state is not the simplest, but may be the most flexible strategy. We suggest that this flexible ancestral strategy may have allowed rapid response to changing environmental conditions which might explain the diversity in parental care strategies that we see in the digger wasps today.
... S1-S4, and Tables S1-S4). We aligned RNA sequences from two previous studies of M. genalis to this genome assembly to investigate the mechanistic links between development and eusociality (53,54). Specifically, we tested the hypothesis that eusociality evolves from existing genes that regulate development by comparing gene-expression changes among life stages and sexes (53), with gene-expression differences among social phenotypes within a single life stage and sex (54) (Fig. 1B). ...
... We aligned RNA sequences from two previous studies of M. genalis to this genome assembly to investigate the mechanistic links between development and eusociality (53,54). Specifically, we tested the hypothesis that eusociality evolves from existing genes that regulate development by comparing gene-expression changes among life stages and sexes (53), with gene-expression differences among social phenotypes within a single life stage and sex (54) (Fig. 1B). We approached this hypothesis from a transcriptomic perspective because co-option of developmental pathways for novel functions is likely to involve shifts in gene expression (2,10). ...
... We additionally found that socially expressed genes are under positive selection, indicating that the regulation of genes related to social behavior is adaptively shaped by evolution in this ancestral proxy population. Moreover, caste-biased genes in M. genalis have been previously shown to be under strong positive selection in obligately eusocial species, suggesting that there has been adaptive refinement of these genes in derived lineages (54). Our study thus provides the missing pieces of an emerging picture for plasticity-led social evolution in a facultatively eusocial bee. ...
Article
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Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in caste-based (eusocial) societies are particularly sensitive to developmental processes, and the evolutionary origins of eusociality may be rooted in developmental plasticity of ancestral forms. We used an integrative genomics approach to evaluate the relationships among developmental plasticity, molecular evolution, and social behavior in a bee species ( Megalopta genalis ) that expresses flexible sociality, and thus provides a window into the factors that may have been important at the evolutionary origins of eusociality. We find that differences in social behavior are derived from genes that also regulate sex differentiation and metamorphosis. Positive selection on social traits is influenced by the function of these genes in development. We further identify evidence that social polyphenisms may become encoded in the genome via genetic changes in regulatory regions, specifically in transcription factor binding sites. Taken together, our results provide evidence that developmental plasticity provides the substrate for evolutionary novelty and shapes the selective landscape for molecular evolution in a major evolutionary innovation: Eusociality.
... Ongoing comparative research involving Hymenoptera which demonstrate non-eusocial forms of social organization (i.e. incipient sociality) is rapidly advancing our understanding of the molecular and environmental factors that may have contributed to the emergence and elaboration of sociality [20][21][22] (reviewed in [19,23]). These works have revealed that, similar to what has been observed among advanced eusocial Hymenoptera, transcriptomic rifts may be forming within these less socially derived species, dividing nest-mates along behavioural and ontogenetic lines (e.g. ...
... These works have revealed that, similar to what has been observed among advanced eusocial Hymenoptera, transcriptomic rifts may be forming within these less socially derived species, dividing nest-mates along behavioural and ontogenetic lines (e.g. Ceratina australensis [18]; Megalopta genalis [20]; Polistes canadensis [24]). These are critical and evolutionarily consequential delineations, as they signify a regulatory separation of gene sets indicative of distinct phenotypic states and/or ontogenetic trajectories; a process of molecular compartmentalization necessary for the reduction (and eventual removal) of ancestral pleiotropic constraints putatively antecedent to a developmentally canalized division of labour [1,25]. ...
... Recent evidence has also provided support for the social ladder hypothesis, which states that differentially expressed and deeply conserved genes probably play an important role in both the early and later stages of social evolution [19,20,26,27]. For example, many of the same genes and regulatory elements that underlie advanced eusocial division of labour in A. mellifera play a conserved role in the incipiently social Australian small carpenter bee (C. ...
Article
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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.
... Other researchers [29][30][31], acknowledging that it is impossible to directly study the evolution of traits that evolved millions of years ago, explicitly argue that a powerful workaround is to pick an extant 'ancestor proxy' species that has certain ancestral traits (e.g. solitary life history) and assume that it is a living representative of the long-extinct ancestor of a second extant, phylogenetically related species with certain derived traits (e.g. ...
... complex eusociality). Comparisons between the two extant species are then made as a means to elucidate the evolution and molecular underpinnings of the derived trait(s) [29][30][31]. We note that this approach immediately begs the question of which extant species might be a good (or the best) ancestor proxy, given that any evolutionary or genetic inferences may strongly depend on the specific choice, since species often vary widely due to local adaptation, historical contingency, and so on. ...
... Extant groups (e.g. various apid bee genera, illustrated here) at different locations in trait space are then assumed to reflect different stages of social evolution [11,16]; the ancestors of groups with higher social complexity is assumed to have historically passed through locations in phenotypic space occupied by groups with lower social complexity; and extant groups with lower social complexity are assumed to reflect the ancestor of groups with higher social complexity [30,31]. Note that in reality, the apid groups illustrated here vary widely in measures of social complexity, so that for example, the illustrated location of Melipona in trait space might reflect the location of a single species or the genus mean, but other related species and genera would likely be in different regions of trait space. ...
Article
The evolution of large insect societies is a major evolutionary transition that occurred in the long-extinct ancestors of termites, ants, corbiculate bees, and vespid wasps. Researchers have long used 'social ladder thinking': assuming progressive stepwise phenotypic evolution and asserting that extant species with simple societies (e.g. some halictid bees) represent the ancestors of species with complex societies, and thus provide insight into general early steps of eusocial evolution. We discuss how this is inconsistent with data and modern evolutionary 'tree thinking'. Phylogenetic comparative methods with broad sampling provide the best means to make rigorous inferences about ancestral traits and evolutionary transitions that occurred within each lineage, and to determine whether consistent phenotypic and genomic changes occurred across independent lineages.
... B 286: 20190588 addition, we included genes known to be associated with hormone sensitivity, insect behavioural plasticity, or caste determination (electronic supplementary material, table S5, [26 -31]). We also compared the DEG lists identified in our study to other published data obtained for Megalopta genalis [32] and Apis mellifera [33][34][35]. These comparisons represent independent origins of eusociality and correspond to different degrees of eusocial complexity. ...
... By contrast, M. genalis has a similar life history to E. dilemma even though it represents an independent origin of eusociality [36]. For comparisons to M. genalis, we identified orthologous genes between the published E. dilemma peptide set and the predicted TransDecoder peptides from Jones et al. [32] using a reciprocal best hit (RBH) blastp search (e-value ,1Â10 25 ). For A. mellifera comparisons, we converted our E. dilemma gene lists into honeybee identifiers (OGSv 3.2; [37]) using a conversion list generated in Brand et al. [21]. ...
Article
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The evolution of eusociality and sterile worker castes represents a major transition in the history of life. Despite this, little is known about the mechanisms involved in the initial transition from solitary to social behaviour. It has been hypothesized that plasticity from ancestral solitary life cycles was coopted to create queen and worker castes in insect societies. Here, we tested this hypothesis by examining gene expression involved in the transition from solitary to social behaviour in the orchid bee Euglossa dilemma. To this end, we conducted observations that allowed us to classify bees into four distinct categories of solitary and social behaviour. Then, by sequencing brain and ovary transcriptomes from these behavioural phases, we identified gene expression changes overlapping with socially associated genes across multiple eusocial lineages. We find that genes involved in solitary E. dilemma ovarian plasticity overlap extensively with genes showing differential expression between fertile and sterile workers-or between queens and workers in other eusocial bees. We also find evidence that sociality in E. dilemma reflects gene expression patterns involved in solitary foraging and non-foraging nest care behaviours. Our results provide strong support for the hypothesis that eusociality emerges from plasticity found across solitary life cycles.
... Solitary nests arise when the female produces all sons in her brood, while social nests arise when at least one daughter stays at the nest as a worker instead of dispersing (Wcislo et al. 2004;Wcislo and Gonzalez 2006;Chambers et al. 2007). Gene expression in the abdomens of facultatively eusocial M. genalis is caste-specific, and upregulated genes are rapidly evolving and have likely been targets of selection in obligately eusocial species (Jones et al. 2017). Eusociality may have been ancestrally plastic, with this plasticity later followed by changes in gene regulation and adaptive refinement (plasticity-led evolution; see Levis and Pfennig 2021). ...
... The potential importance of plasticity in two other evolutionary transitions in individuality introduced in Table 10.1-namely, the origin of the genome and origin of eukaryotes-also requires additional research. Concerning the evolution of eusocial insect societies, researchers have posited that eusociality was ancestrally facultative before coming under genetic control in some lineages (e.g., Jones et al. 2017;Jones and Robinson 2018). Plasticity in caste development has been well-characterized and is uncontroversial (reviewed in Corona et al. 2016). ...
... As with the evolution of the metazoan immune system, which is thought to have emerged via the co-option of preexisting molecular modules and functions into novel defensive pathways, it has been hypothesized that social immune systems originated via similar processes [10], with a potentially crucial role for behavioural [11] as well as immune gene adaptations [12,13]. In line with this view, many genes, including immune-related genes, have been shown to display castespecific expression patterns [14][15][16][17][18]. In addition, enhanced antimicrobial defences have been recorded in some social insects compared with their solitary relatives [2][3][4]19]. ...
... The social insect colony is a highly organized society with specialized castes. Previous studies in termites have revealed caste-specific expression patterns that reflect functional specialization of castes [14][15][16][17][18]. We found that constitutive immune gene expression is strongly caste specific in N. castaneus, reflecting a division of social roles and indicating a significant degree of caste-specific immune defence. ...
Article
The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.
... Females that pursue a solitary strategy are smaller, with lower titers of juvenile hormone, and reach reproductive maturity later than females pursuing a social strategy Smith et al. 2013). However, there are relatively few differentially expressed genes in the abdomens and brains of solitary females and queens (Jones et al. 2017). Additional research is necessary to determine whether there are differences in maternal gene expression specifically associated with rearing future queens and future workers in facultatively social species. ...
... Species which exhibit facultative eusociality, such as the sweat bee M. genalis, can be studied as proxies for the ancestral state from which sociality evolved. Jones et al. (2017) used this approach to identify environmentally induced plasticity that may have preceded adaptive social evolution. They found that genes which are differentially expressed in one or more reproductive and social castes in M. genalis significantly overlap with caste-biased genes in obligately eusocial bees from different lineages, spanning multiple origins of sociality. ...
Article
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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.
... caste) were compared against targets of lineage-specific miRNAs (electronic supplementary material, table S5). For M. genalis caste data, RNAseq reads from Jones et al. [41] (NCBI PRJNA331103) were trimmed using Trimmomatic (v. 0.36) [42] and aligned to a draft genome assembly of M. genalis (NCBI PRJNA494872) [35] using STAR (v. ...
... Gene counts were obtained using featureCounts in the Subread package (v. 1.5.2) [44], and differential expression analysis was conducted using edgeR [45] as in Jones et al. [41]. ...
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Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20–35%) of detected miRNAs had lineage-specific expression in the brain, 24–72% of which did not have homologues in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.
... When trying to understand the evolution of eusociality, a major and on-going question could be simplistically framed as a 'chicken-or-egg' problem: did worker castes arise before helper sterility, or did effective sterility allow worker morphologies to evolve later on? That issue cannot be readily addressed using taxa such as ants, termites or honeybees because they do not contain extant species that might approximate conditions when sociality was first evolving [4,12]. Instead, we need to examine species where sociality has only recently evolved and where altruistic behaviour is not obligate. ...
Article
To understand the earliest stages of social evolution, we need to identify species that are undergoing the initial steps into sociality. Amphylaeus morosus is the only unambiguously known social species in the bee family Colletidae and represents an independent origin of sociality within the Apoidea. This allows us to investigate the selective factors promoting the transition from solitary to social nesting. Using genome-wide SNP genotyp-ing, we infer robust pedigree relationships to identify maternity of brood and intracolony relatedness for colonies at the end of the reproductive season. We show that A. morosus forms both matrifilial and full-sibling colonies, both involving complete or almost complete monopolization over reproduction. In social colonies, the reproductive primary was also the primary forager with the secondary female remaining in the nest, presumably as a guard. Social nesting provided significant protection against parasitism and increased brood survivorship in general. We show that secondary females gain large indirect fitness benefits from defensive outcomes, enough to satisfy the conditions of inclusive fitness theory, despite an overproduction of males in social colonies. These results suggest an avenue to sociality that involves high relatedness and, very surprisingly, extreme reproductive skew in its earliest stages and raises important questions about the evolutionary steps in pathways to eusociality.
... Thus, it might be of benefit to use these housekeeping genes to study gene expression in primitively eusocial species like Euglossini bees, especially because recent studies showed that there are major dissimilarities between ages and environment (Lockett et al., 2016), in different tissues (e.g. brain and abdomen), and between solitary and eusocial bee species with respect to transcriptional regulation (Jones et al., 2017;Kapheim et al., 2015). ...
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Studies on the expression of genes in different contexts are essential to our understanding of the functioning of organisms and their adaptations to the environment. Gene expression studies require steps of normalization, which are done using the stable expression pattern of reference genes. For many different eusocial bees reference genes have been discovered, but not for the primitively eusocial Euglossini bees. We used available genomic resources of Euglossini species and the gene information of Apis mellifera Linnaeus to develop a set of reference genes for the primitive eusocial bee Euglossa viridissima Friese. We tested nine genes, in distinct developmental stages, using three different algorithms, to infer stability of gene expression. The TATA-binding protein (TBP) and 14-3-3 epsilon were the most stable genes across all developmental stages. The strongest deviation in gene expression pattern occurred in pupae, which require a different set of genes for normalizing gene expression.
... This means that just as changes in gene expression drive cell type specifications, they should also drive developmentally-determined caste differentiation in the social insects. There is growing evidence to support this assertion, including well-documented changes in gene expression in developing larvae and in adults [12][13][14][15][16][17][18][19][20][21][22], as well as changes in DNA methylation [23][24][25][26], post-translational histone modifications, and chromatin accessibility [27][28][29]. ...
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The evolution of eusociality represents an increase in complexity from individual to caste-based, group reproduction. These behavioral transitions have been hypothesized to go hand-in-hand with an increased ability to regulate when and where genes are expressed. Bees have convergently evolved eusociality up to five times, providing a powerful framework to test this hypothesis. Here, we compare conserved, non-coding sequences in eleven bee species, encompassing three independent origins of reproductive division of labor and two elaborations of eusocial complexity to examine potential links between these putatively regulatory sequences and social evolution. We find that rates of evolution in a number of these loci are correlated with social transitions, suggesting they have played a role in the evolution of these behaviors. Interestingly, loci associated with social origins represent distinct molecular pathways to those associated with subsequent elaborations. We also find many novel non-coding regions that appear to have been recruited alongside the origin of sociality in corbiculate bees; these regions are enriched for cell development and nervous system functions. Thus, our results highlight the potential importance of non-coding change in the evolution of eusociality and are consistent with the idea that regulatory innovations play a key role in insect behavioral complexity.
... Most of these studies have either focused on the brain or whole-body samples 15,22,24,26,33,[35][36][37] , although expression bias between queens and workers has been shown to be dependent upon developmental stage and tissue type 34,[38][39][40] . Finally, the transcriptomic signatures of reproductive physiology are strongest in the abdomen 34,41 , the location of reproductive organs, but no past study has explicitly compared caste bias in abdominal tissues in species from lineages representing independent origins of eusociality. ...
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Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown. Here we characterize caste-specific transcriptomic profiles across development and adult body segments from pharaoh ants (Monomorium pharaonis) and honey bees (Apis mellifera), representing two independent origins of eusociality. We identify a substantial shared core of genes upregulated in the abdomens of queen ants and honey bees that also tends to be upregulated in mated female flies, suggesting that these genes are part of a conserved insect reproductive groundplan. Outside of this shared groundplan, few genes are differentially expressed in common. Instead, the majority of the thousands of caste-associated genes are plastically expressed, rapidly evolving, and relatively evolutionarily young. These results emphasize that the recruitment of both highly conserved and lineage-specific genes underlie the convergent evolution of novel traits such as eusociality.
... http://dx.doi.org/10.1101/730317 doi: bioRxiv preprint first posted online brain gene expression patterns between queen and worker honey bees (thousands of genes; 561 Grozinger et al. 2007) and M. genalis (dozens of genes; Jones et al. 2017). Previous research 562 suggests that miRNAs increase their functional influence over evolutionary time (Berezikov et 563 al. 2006;Chen and Rajewsky 2007;Lu et al. 2008;Roux et al. 2012;França et al. 2016;Patel 564 and Capra 2017). ...
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Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are largely unknown. We tested the hypothesis that changes in gene regulatory function associated with social evolution are facilitated by lineage-specific microRNA (miRNA) regulatory function. Genome scans across 12 bees showed that miRNA copy number is highly conserved and is not associated with variation in social organization. However, deep sequencing of small RNAs of six bee species revealed a substantial proportion (20-35%) of miRNAs are expressed in the brains of a single species, and many of these do not have identifiable homologs in any other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than more evolutionarily conserved miRNAs. Consistent with our hypothesis, the predicted targets of lineage-specific miRNAs are enriched for genes related to social behavior, such as caste-biased genes, in social species, but they are either not enriched for or significantly depleted of genes under positive selection. Together, these results suggest that novel miRNAs may contribute to lineage-specific patterns of molecular evolution associated with the origins and elaborations of eusociality. Our analyses also lend support to earlier hypotheses concerning miRNA origins from a relatively understudied taxonomic group, and reveal important differences in the evolution and assimilation of novel miRNAs between mammals and insects.
... It also serves to illuminate the basis of the major transition entailed by the evolution of eusociality (Bourke, 2011). For these reasons, several studies have isolated caste-associated genes in eusocial Hymenoptera using microarrays or mRNA-seq to profile adult queens and workers (Feldmeyer et al., 2014;Ferreira et al., 2013;Grozinger et al., 2007;Harrison et al., 2015;Jones et al., 2017;Kapheim et al., 2020;Niu et al., 2014;Toth et al., 2010;Woodard et al., 2014). ...
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The queen‐worker caste system of eusocial insects represents a prime example of developmental polyphenism (environmentally‐induced phenotypic polymorphism) and is intrinsic to the evolution of advanced eusociality. However, the comparative molecular basis of larval caste determination and subsequent differentiation in the eusocial Hymenoptera remains poorly known. To address this issue within bees, we profiled caste‐associated gene expression in female larvae of the intermediately eusocial bumblebee Bombus terrestris. In B. terrestris, female larvae experience a queen‐dependent period during which their caste fate as adults is determined followed by a nutrition‐sensitive period also potentially affecting caste fate but for which the evidence is weaker. We used mRNA‐seq and qRT‐PCR validation to isolate genes differentially expressed between each caste pathway in larvae at developmental stages before and after each of these periods. We show that differences in gene expression between caste pathways are small in totipotent larvae, then peak after the queen‐dependent period. Relatively few novel (i.e. taxonomically‐restricted) genes were differentially expressed between castes, though novel genes were significantly enriched in late‐instar larvae in the worker pathway. We compared sets of caste‐associated genes in B. terrestris with those reported from the advanced eusocial honeybee, Apis mellifera, and found significant but relatively low levels of overlap of gene lists between the two species. These results suggest both the existence of low numbers of shared toolkit genes and substantial divergence in caste‐associated genes between Bombus and the advanced eusocial Apis since their last common eusocial ancestor.
... Facultatively eusocial insects provide a powerful means of assessing the ecological factors that favor the evolution of eusociality (Purcell 2011;Wcislo 1997), as well as the genetic and physiological mechanisms that underpin its expression (Jones et al. 2017;Schwarz et al. 2007). As yet, however, queen pheromones have not been identified for any facultatively eusocial species. ...
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Queen pheromones evolved independently in multiple eusocial insect lineages, in which they mediate reproductive conflict by inhibiting worker ovarian development. Although fundamentally important for reproductive division of labor – the hallmark of eusociality – their evolutionary origins are enigmatic. Here, we analyze cuticular and Dufour’s gland chemistries across alternative social and reproductive phenotypes in Megalopta genalis bees (tribe Augochlorini, family Halictidae) that facultatively express simple eusociality. Reproductive bees have distinct overall glandular and cuticular chemical phenotypes compared with non-reproductive workers. On the cuticle, a likely site of signal transmission, reproductives are enriched for certain alkenes, most linear alkanes, and are heavily enriched for all methyl-branched alkanes. Chemicals belonging to these compound classes are known to function as fertility signals in other eusocial insect taxa. Some macrocyclic lactones, compounds that serve as queen pheromones in the other eusocial halictid tribe (Halictini), are also enriched among reproductives relative to workers. The intra-population facultative eusociality of M. genalis permits direct comparisons between individuals expressing alternative reproductive phenotypes – females that reproduce alone (solitary reproductives) and social queens – to highlight traits in the latter that may be important mediators of eusociality. Compared with solitary reproductives, the cuticular chemistries of queens are more strongly differentiated from those of workers, and furthermore are especially enriched for methyl-branched alkanes. Determining the pheromonal function(s) and information content of the candidate signaling compounds we identify will help illuminate the early evolutionary history of queen pheromones, chemical signals central to the organization of insect eusocial behavior.
... crustacean | ddRAD | sociality | genome architecture | transposon E usociality is defined by a reproductive division of labor where some individuals forego independent breeding to cooperatively rear others' young (1). Recent advances in molecular biology have enabled researchers to begin to uncover the genomic underpinnings of eusociality by identifying associated genetic variants and pathways (2)(3)(4) and highlighting the importance of recombination (5), gene regulation (6), novel genes (7), genetic accommodation (8), epigenetics (9,10), and developmental plasticity (11)(12)(13) in the transition toward social complexity. Yet, more recently there has been a shift toward also considering the phenotypic (14,15), demographic (16)(17)(18), and genomic consequences (17,19) of living in complex social groups. ...
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Despite progress uncovering the genomic underpinnings of sociality, much less is known about how social living affects the genome. In different insect lineages, for example, eusocial species show both positive and negative associations between genome size and structure, highlighting the dynamic nature of the genome. Here, we explore the relationship between sociality and genome architecture in Synalpheus snapping shrimps that exhibit multiple origins of eusociality and extreme interspecific variation in genome size. Our goal is to determine whether eusociality leads to an accumulation of repetitive elements and an increase in genome size, presumably due to reduced effective population sizes resulting from a reproductive division of labor, or whether an initial accumulation of repetitive elements leads to larger genomes and independently promotes the evolution of eusociality through adaptive evolution. Using phylogenetically informed analyses, we find that eusocial species have larger genomes with more transposable elements (TEs) and microsatellite repeats than noneusocial species. Interestingly, different TE subclasses contribute to the accumulation in different species. Phylogenetic path analysis testing alternative causal relationships between sociality and genome architecture is most consistent with the hypothesis that TEs modulate the relationship between sociality and genome architecture. Although eusociality appears to influence TE accumulation, ancestral state reconstruction suggests moderate TE abundances in ancestral species could have fueled the initial transitions to eusociality. Ultimately, we highlight a complex and dynamic relationship between genome and social evolution, demonstrating that sociality can influence the evolution of the genome, likely through changes in demography related to patterns of reproductive skew.
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Agonistic interactions among individuals can result in the formation of dominance hierarches that can reinforce individual behavior and social status. Such dominance hierarches precede the establishment of reproductive dominance, division of labor, and caste formation in highly social insect taxa. As such, deciphering the molecular basis of aggression is fundamental in understanding the mechanisms of social evolution. Assessing the proximate mechanisms of aggression in incipiently social bees can provide insights into the foundations of genomic mechanisms of social behavior. Here, we measured the effects of aggression on brain gene expression in the incipiently social bee, Ceratina australensis. We examine the brain transcriptomic differences between individuals who have experienced recurrent winning, losing, or a change in rank during repeated encounters. Using comparative analyses across taxa, we identify deeply conserved candidate genes, pathways, and regulatory networks for the formation of social hierarchies. This article is protected by copyright. All rights reserved. Expression profiles for aggression in social Hymenoptera and vertebrates reveal conserved genes underlying dominance behavior
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Eusociality has evolved multiple times across the insect phylogeny. Social insects with greater levels of social complexity tend to exhibit specialized castes with low levels of individual phenotypic plasticity. In contrast, species with simple social groups may consist of totipotent individuals that transition among behavioral and reproductive states. However, recent work has shown that in simple social groups, there can still be constraint on individual plasticity, caused by differences in maternal nourishment or social interaction. It is not well understood how these constraints arise, ultimately leading to the evolution of nonreproductive workers. Some species of orchid bees form social groups of a dominant and 1–2 subordinate helpers where all individuals are reproductive. Females can also disperse to start their own nest as a solitary foundress, which includes a nonreproductive phase, characterized by ovary inactivation, not typically expressed by subordinates. Little is known about individual flexibility across these trajectories. Here, using the orchid bee Euglossa dilemma, we assess the plasticity of subordinate helpers, finding that they are capable of the same behavioral, physiological, transcriptomic, and chemical changes seen in foundresses. Our results suggest that the lack of nonreproductive workers in E. dilemma is not due to a lack of subordinate plasticity. This article is protected by copyright. All rights reserved
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The evolutionary origins of eusociality represent increases in complexity from individual to caste-based, group reproduction. These behavioural transitions have been hypothesized to go hand in hand with an increased ability to regulate when and where genes are expressed. Bees have convergently evolved eusociality up to five times, providing a framework to test this hypothesis. To examine potential links between putative gene regulatory elements and social evolution, we compare alignable, non-coding sequences in 11 diverse bee species, encompassing three independent origins of reproductive division of labour and two elaborations of eusocial complexity. We find that rates of evolution in a number of non-coding sequences correlate with key social transitions in bees. Interestingly, while we find little evidence for convergent rate changes associated with independent origins of social behaviour, a number of molecular pathways exhibit convergent rate changes in conjunction with subsequent elaborations of social organization. We also present evidence that many novel non-coding regions may have been recruited alongside the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements associated with division of labour within this group. Thus, our findings are consistent with the hypothesis that gene regulatory innovations are associated with the evolution of eusociality and illustrate how a thorough examination of both coding and non-coding sequence can provide a more complete understanding of the molecular mechanisms underlying behavioural evolution. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.
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The study of the major transition to eusociality presents several challenges to researchers, largely resulting from the importance of complex behavioral phenotypes and the shift from individual to group level selection. These challenges are being met with corresponding technological improvements. Advances in resource development for non-model taxa, behavioral tracking, nucleic acid sequencing, and reverse genetics are facilitating studies of hypotheses that were previously intractable. These innovations are resulting in the development of new model systems tailored to the exploration of specific behavioral phenotypes and the querying of underlying molecular mechanisms that drive eusocial behaviors. Here, we present a brief overview of how methodological innovations are advancing our understanding of the evolution of eusociality.
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The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well studied immunity at the cell and individual level, little is known about the origins of immunity during the transition to eusociality,a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We identified five significant immune gene family contractions and one immune gene family expansion along the spine of a time-calibrated phylogeny, correlating with key transitions in termite sociality. In cross-species comparisons of immune gene expression, we find that termites appear to have evolved a caste-specific social defense system at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity entailed a fundamental reshaping of the immune system optimized for group over individual defense.
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Understanding the regulatory architecture of phenotypic variation is a fundamental goal in biology, but connections between gene regulatory network (GRN) activity and individual differences in behavior are poorly understood. We characterized the molecular basis of behavioral plasticity in queenless honey bee ( Apis mellifera ) colonies, where individuals engage in both reproductive and non-reproductive behaviors. Using high-throughput behavioral tracking, we discovered these colonies contain a continuum of phenotypes, with some individuals specialized for either egg-laying or foraging and ‘generalists’ that perform both. Brain gene expression and chromatin accessibility profiles were correlated with behavioral variation, with generalists intermediate in behavior and molecular profiles. Models of brain GRNs constructed for individuals revealed that transcription factor (TF) activity was highly predictive of behavior, and behavior-associated regulatory regions had more TF motifs. These results provide new insights into the important role played by brain GRN plasticity in the regulation of behavior, with implications for social evolution.
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Queens and workers of eusocial Hymenoptera are considered homologous to the reproductive and brood care phases of an ancestral subsocial life cycle. However, the molecular mechanisms underlying the evolution of reproductive division of labor remain obscure. Using a brain transcriptomics screen, we identified a single gene, insulin-like peptide 2 (ilp2), which is always up-regulated in ant reproductives, likely because they are better nourished than their nonreproductive nestmates. In clonal raider ants (Ooceraea biroi), larval signals inhibit adult reproduction by suppressing ilp2, thus producing a colony reproductive cycle reminiscent of ancestral subsociality. However, increasing ILP2 peptide levels overrides larval suppression, thereby breaking the colony cycle and inducing a stable division of labor. These findings suggest a simple model for the origin of ant eusociality via nutritionally determined reproductive asymmetries potentially amplified by larval signals.
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Understanding the evolutionary origins of social behavior in insects requires understanding the physiological basis for reproductive plasticity. Solitary bees and wasps, or those living in small, flexible societies, will be key to understanding how conserved pathways have evolved to give rise to reproductive castes. Nutrient-sensing and endocrine pathways are decoupled from reproduction in some life stages of social insects. Heterochrony, particularly as it is related to diapause physiology, may be an important mechanism by which this decoupling occurs. Additional research is needed to understand how these pathways became sensitive to cues from the social environment. Future research targeting species with a diversity of social behaviors and diapause strategies will be key to understanding the physiological basis of social evolution.
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Comparative genomics of social insects has been intensely pursued in recent years with the goal of providing insights into the evolution of social behavior and its underlying genomic and epigenomic basis. However, the comparative approach has been hampered by a paucity of data on some of the most informative social forms (e.g. incipiently and primitively social) and taxa (especially members of the paper wasp family Vespidae) for studying social evolution. Here we provide a draft genome of the primitively eusocial model insect Polistes dominula, accompanied by analysis of caste-related transcriptome and methylome sequence data for adult queens and workers. P. dominula possesses a fairly typical hymenopteran genome, but shows very low genome-wide GC content and some evidence of reduced genome size. We found numerous caste-related differences in gene expression, with evidence that both conserved and novel genes are related to caste differences. Most strikingly, these -omics data reveal a major reduction in one of the major epigenetic mechanisms that has been previously suggested to be important for caste differences in social insects: DNA methylation. Along with a conspicuous loss of a key gene associated with environmentally responsive DNA methylation (the de novo DNA methyltransferase Dnmt3), these wasps have greatly reduced genome-wide methylation to almost zero. In addition to providing a valuable resource for comparative analysis of social insect evolution, our integrative -omics data for this important behavioral and evolutionary model system call into question the general importance of DNA methylation in caste differences and evolution in social insects. This article is protected by copyright. All rights reserved.
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Sexual reproduction brings genes from two parents (matrigenes and patrigenes) together into one individual. These genes, despite being unrelated, should show nearly perfect cooperation because each gains equally through the production of offspring. However, an individual's matrigenes and patrigenes can have different probabilities of being present in other relatives, so kin selection could act on them differently. Such intragenomic conflict could be implemented by partial or complete silencing (imprinting) of an allele by one of the parents. Evidence supporting this theory is seen in offspring-mother interactions, with patrigenes favoring acquisition of more of the mother's resources if some of the costs fall on half-siblings who do not share the patrigene. The kinship theory of intragenomic conflict is little tested in other contexts, but it predicts that matrigene-patrigene conflict may be rife in social insects. We tested the hypothesis that honey bee worker reproduction is promoted more by patrigenes than matrigenes by comparing across nine reciprocal crosses of two distinct genetic stocks. As predicted, hybrid workers show reproductive trait characteristics of their paternal stock, (indicating enhanced activity of the patrigenes on these traits), greater patrigenic than matrigenic expression, and significantly increased patrigenic-biased expression in reproductive workers. These results support both the general prediction that matrigene-patrigene conflict occurs in social insects and the specific prediction that honey bee worker reproduction is driven more by patrigenes. The success of these predictions suggests that intragenomic conflict may occur in many contexts where matrigenes and patrigenes have different relatednesses to affected kin.
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Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.
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Transcriptomes provide excellent foundational resources for mechanistic and evolutionary analyses of complex traits. We present a developmental transcriptome for the facultatively eusocial bee Megalopta genalis, which represents a potential transition point in the evolution of eusociality. A de novo transcriptome assembly of Megalopta genalis was generated using paired-end Illumina sequencing and the Trinity assembler. Males and females of all life stages were aligned to this transcriptome for analysis of gene expression profiles throughout development. Gene Ontology analysis indicates that stage-specific genes are involved in ion transport, cell-cell signaling, and metabolism. A number of distinct biological processes are upregulated in each life stage and transitions between life stages involve shifts in dominant functional processes, including shifts from transcriptional regulation in embryos to metabolism in larvae, and increased lipid metabolism in adults. We expect that this transcriptome will provide a useful resource for future analyses to better understand the molecular basis of the evolution of eusociality, and more generally, phenotypic plasticity. Copyright © 2015 Author et al.
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Genomic tools are allowing us to dissect the roles of genes and genetic architecture in social evolution, and eusocial insects are excellent models. Numerous hypotheses for molecular evolution of eusociality have been proposed, ranging from regulatory shifts in 'old' genes to rapid evolution of 'new' genes. A broad model to explain this major transition in evolution has been lacking. We provide a synthetic framework centered on the idea that different evolutionary processes dominate during different transitional stages, beginning with changes in gene regulation and culminating in novel genes later on. By considering multiple mechanisms as we 'climb the social ladder', we can test whether the transitions from solitary to simple sociality to complex sociality represent incremental changes or genetic revolutions. Copyright © 2015 Elsevier Ltd. All rights reserved.
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The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of ten bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.
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The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of ten bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.
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An area of great interest in evolutionary genomics is whether convergently evolved traits are the result of convergent molecular mechanisms. The presence of queen and worker castes in insect societies is a spectacular example of convergent evolution and phenotypic plasticity. Multiple insect lineages have evolved environmentally induced alternative castes. Given multiple origins of eusociality in Hymenoptera (bees, ants, and wasps), it has been proposed that insect castes evolved from common genetic “toolkits” consisting of deeply conserved genes. Here, we combine data from previously published studies on fire ants and honey bees with new data for Polistes metricus paper wasps to assess the toolkit idea by presenting the first comparative transcriptome-wide analysis of caste determination among three major hymenopteran social lineages. Overall, we found few shared caste differentially expressed transcripts across the three social lineages. However, there is substantially more overlap at the levels of pathways and biological functions. Thus, there are shared elements but not on the level of specific genes. Instead, the toolkit appears to be relatively “loose,” that is, different lineages show convergent molecular evolution involving similar metabolic pathways and molecular functions but not the exact same genes. Additionally, our paper wasp data do not support a complementary hypothesis that “novel” taxonomically restricted genes are related to caste differences.
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Bees are excellent models for studying the evolution of sociality. While most species are solitary, many form social groups. The most complex form of social behavior, eusociality, has arisen independently four times within the bees. Subsequent elaborations of the reproductive division of labor inherent to eusociality have led to the evolution of some of the most highly advanced forms of eusociality documented. Likewise, many reversals back to solitary behavior also create substantial variation in sociality within the bees. These replicated, independent origins and losses enable a comparative approach that facilitates the search for common mechanisms underlying transitions from solitary to group living. In this review, we discuss the extensive behavioral variation found within the bees and highlight how the comparative method has improved our understanding of social evolution. Finally, we discuss potential difficulties with this approach and outline promising avenues for future research. comparative method / evolution / communal / semisocial / eusocial / genetics / genomics
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Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea- and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.
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The reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality.
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In tropical monsoon forest of Barro Colorado Island, 50 species and 17 genera have been recorded. Most bees were Megalopta; these species were present throughout the year, as were Rhinetula and Ptiloglossa. Abundance of Megalopta was lowest during the dry season; this was its only consistent seasonality. Peak abundance occurred at various times during dry-to-wet-season transition and in the 1st half and the end of the wet season. Centris and Epicharis, large, solitary anthophorid bees, were present in the early wet season and absent in the late wet season and most of the dry season. The highly social bee Trigona aff. cupira was aseasonal but had abundance peaks during all but the mid-to-late wet season. Megalopta genalis abundance and M. ecuadoria abundance were highly positively correlated within years, and weakly correlated with abundances of other bees. Pairwise correlations between years were low for each Megalopta species and for combined bees of other genera. -from Authors
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Background Understanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution. Results We sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways. Conclusions These genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.
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The data and tools in PANTHER—a comprehensive, curated database of protein families, trees, subfamilies and functions available at http://pantherdb.org—have undergone continual, extensive improvement for over a decade. Here, we describe the current PANTHER process as a whole, as well as the website tools for analysis of user-uploaded data. The main goals of PANTHER remain essentially unchanged: the accurate inference (and practical application) of gene and protein function over large sequence databases, using phylogenetic trees to extrapolate from the relatively sparse experimental information from a few model organisms. Yet the focus of PANTHER has continually shifted toward more accurate and detailed representations of evolutionary events in gene family histories. The trees are now designed to represent gene family evolution, including inference of evolutionary events, such as speciation and gene duplication. Subfamilies are still curated and used to define HMMs, but gene ontology functional annotations can now be made at any node in the tree, and are designed to represent gain and loss of function by ancestral genes during evolution. Finally, PANTHER now includes stable database identifiers for inferred ancestral genes, which are used to associate inferred gene attributes with particular genes in the common ancestral genomes of extant species.
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The evolution of eusociality is hypothesized to have involved de-coupling parental care from reproduction mediated by changes in endocrine regulation. While data for obligately eusocial insects are consistent with this hypothesis, we lack information from species representative of the transition from solitary reproduction to eusociality. Here we report the first evidence for a link between endocrine processes and social behavior in a facultatively eusocial bee, Megalopta genalis (Halictidae). Using females that varied in social, reproductive, and ecological context, we measured juvenile hormone (JH), a major regulator of colony caste dynamics in other eusocial species. JH was low at adult emergence, but elevated after 10days in all nesting females. Females reared in cages with ad lib nutrition, however, did not elevate JH levels after 10days. All reproductive females had significantly more JH than all age-matched non-reproductive females, suggesting a gonadotropic function. Among females in established nests, JH was higher in queens than workers and solitary reproductives, suggesting a role for JH in social dominance. A lack of significant differences in JH between solitary reproductives and non-reproductive workers suggests that JH content reflects more than reproductive status. Our data support the hypothesis that endocrine modifications are involved in the evolutionary decoupling of reproductive and somatic effort in social insects. These are the first measurements of JH in a solitary-nesting hymenopteran, and the first to compare eusocial and solitary nesting individuals of the same species.
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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 weak-ly 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 unbi-ased 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 dif-ferences 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 oth-er 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 polymor-phism has both genetic and environmental influences, raising questions as to the relative import of each.
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Gene expression responds to the environment and can also evolve rapidly in response to altered selection regimes. Little is known, however, about the extent to which evolutionary adaptation to a particular type of stress involves changes in the within-generation ('plastic') responses of gene expression to the stress. We used microarrays to quantify gene expression plasticity in response to ethanol in laboratory populations of Drosophila melanogaster differing in their history of ethanol exposure. Two populations ('R' populations) were maintained on regular medium, two ('E') were maintained on medium supplemented with ethanol, and two ('M') were maintained in a mixed regime in which half of the population was reared on one medium type, and half on the other, each generation. After more than 300 generations, embryos from each population were collected and exposed to either ethanol or water as a control, and RNA was extracted from the larvae shortly after hatching. Nearly 2000 transcripts showed significant within-generation responses to ethanol exposure. Evolutionary history also affected gene expression: the E and M populations were largely indistinguishable in expression, but differed significantly in expression from the R populations for over 100 transcripts, the majority of which did not show plastic responses. Notably, in no case was the interaction between selection regime and ethanol exposure significant after controlling for multiple comparisons, indicating that adaptation to ethanol in the E and M populations did not involve substantial changes in gene expression plasticity. The results give evidence that expression plasticity evolves considerably more slowly than mean expression.
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Evolutionary transitions to dim-light foraging (predawn matinal, crepuscular, nocturnal) have occurred repeatedly in bees, and may be associated with an escape from enemies or competitors. To date, however, little information has been available to test these hypotheses. Here we provide the first detailed information on the nesting behaviour of two species of Neotropical, nocturnal sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae). Females are facultatively social or solitary, and construct nests in dead wood. Nocturnal foraging behaviour is bimodal. Bees began foraging after sunset (∼18:30 h) and ceased foraging approximately 1 h later even though nocturnal flowers with pollen were still abundant; a second foraging bout occurred in the predawn morning, which began at ∼04:45 h and ended around sunrise (∼06:15 h) when diurnal-blooming flowers were abundant. Bees are capable of controlled flight in full light. They utilized pollen from both canopy and understory plant species, which have diurnal or nocturnal pollen anthesis. Megalopta nests are attacked by generalist predators such as ants, as well as the endoparasitic fly Melaloncha sp. nov. (Phoridae), the beetle Macrosaigon gracilis (Rhipophoridae), the parasitic wasp Lophostigma cincta (Mutillidae), and the brood parasite Megalopta byroni (Halictidae). Overall nest survivorship rates were comparable to those for diurnal relatives, but rates of cell parasitism for Megalopta (< < 5%) were substantially lower than they are for day-flying relatives, offering some support for the hypothesis that the evolution of nocturnal behaviour enables escape from natural enemies. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 377–387.
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Facultatively solitary and eusocial species allow for direct tests of the benefits of group living. We used the facultatively social sweat bee Megalopta genalis to test several benefits of group living. We surveyed natural nests modified for observation in the field weekly for 5weeks in 2003. First, we demonstrate that social and solitary nesting are alternative behaviors, rather than different points on one developmental trajectory. Next, we show that solitary nests suffered significantly higher rates of nest failure than did social nests. Nest failure apparently resulted from solitary foundress mortality and subsequent brood orphanage. Social nests had significantly higher productivity, measured as new brood cells provisioned during the study, than did solitary nests. After accounting for nest failures, per capita productivity did not change with group size. Our results support key predictions of Assured Fitness Return models, suggesting such indirect fitness benefits favor eusocial nesting in M. genalis. We compared field collections of natural nests to our observation nest data to show that without accounting for nest failures, M. genalis appear to suffer a per capita productivity decrease with increasing group size. Calculating per capita productivity from collected nests without accounting for the differential probabilities of survival across group sizes leads to an overestimate of solitary nest productivity.
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Caste polymorphism, defined as the presence within a colony of two or more morphologically differentiated individuals of the same sex, is an important character of highly eusocial insects both in the Hymenoptera (ants, bees and wasps) and in the Isoptera (termites), the only two groups in the animal kingdom where highly eusocial species occur. Frequently, caste polymorphism extends beyond mere variations in size (although the extent of variations in size can be in the extreme) and is accompanied by allometric variations in certain body parts. How such polymorphism has evolved and why, in its extreme form, it is essentially restricted to the social insects are questions of obvious interest but without satisfactory answers at the present time. I present a hypothesis entitled ‘genetic release followed by diversifying evolution’, that provides potential answers to these questions. I argue that genetic release followed by diversifying evolution is made possible under a number of circumstances. One of them I propose is when some individuals in a species begin to rely on the indirect component of inclusive fitness while others continue to rely largely on the direct component, as workers and queens in social insects are expected to do. Thus when queens begin to rely on workers for most of the foraging, nest building and brood care, and workers begin to rely increasingly on queens to lay eggs—when queen traits and worker traits do not have to be expressed in the same individual—I postulate the relaxation of stabilizing selection and new spurts of directional selection on both queen-trait genes and worker-trait genes (in contrasting directions) leading to caste polymorphism.
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We used the facultatively social sweat bee Megalopta genalis (Halictidae) to test whether body size is associated with social caste. Behavioral observations showed that non-reproductive foragers were significantly smaller than reproductive nest mate queens, and foragers were also smaller than presumed pre-dispersal reproductives. Moreover, among females from field-collected nests without behavioral observations, relative body size correlated with relative ovary size. Reproductive status is not a direct result of body size, as body size was not significantly associated with either ovary size or fecundity among both solitary and social reproductives. Reproductive status is apparently an outcome of social competition for reproductive dominance, and status is influenced by size relative to nest mates. Our study is the first to demonstrate an association of body size with caste expression in a facultatively social species with relatively weak seasonal constraints on independent nesting. Larvae of a parasitic fly (Fiebrigella sp., Chloropidae) consume pollen provisions stored in nest cells of M. genalis and M. ecuadoria. We tested whether fly parasitism of M. genalis reduces body size. Parasitized females are significantly smaller as adults than their unparasitized nestmates. This reduction is of a similar magnitude to the size differences between castes, and has the potential to shape host reproductive options by influencing competition with nest mates. We present data on the prevalence of parasitism from four collections of M. genalis and two collections of M. ecuadoria from Barro Colorado Island, Panama, and La Selva, Costa Rica.
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A fundamental problem in meta-analysis is how to systematically combine information from multiple statistical tests to rigorously evaluate a single overarching hypothesis. This problem occurs in systems biology when attempting to map genomic attributes to complex phenotypes such as behavior. Behavior and other complex phenotypes are influenced by intrinsic and environmental determinants that act on the transcriptome, but little is known about how these determinants interact at the molecular level. We developed an informatic technique that identifies statistically significant meta-associations between gene expression patterns and transcription factor combinations. Deploying this technique for brain transcriptome profiles from ca. 400 individual bees, we show that diverse determinants of behavior rely on shared combinations of transcription factors. These relationships were revealed only when we considered complex and variable regulatory rules, suggesting that these shared transcription factors are used in distinct ways by different determinants. This regulatory code would have been missed by traditional gene coexpression or cis-regulatory analytic methods. We expect that our meta-analysis tools will be useful for a broad array of problems in systems biology and other fields.
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Phenotypic plasticity--the capacity of a single genotype to produce different phenotypes in response to varying environmental conditions--is widespread. Yet, whether, and how, plasticity impacts evolutionary diversification is unclear. According to a widely discussed hypothesis, plasticity promotes rapid evolution because genes expressed differentially across different environments (i.e., genes with "biased" expression) experience relaxed genetic constraint and thereby accumulate variation faster than do genes with unbiased expression. Indeed, empirical studies confirm that biased genes evolve faster than unbiased genes in the same genome. An alternative hypothesis holds, however, that the relaxed constraint and faster evolutionary rates of biased genes may be a precondition for, rather than a consequence of, plasticity's evolution. Here, we evaluated these alternative hypotheses by characterizing evolutionary rates of biased and unbiased genes in two species of frogs that exhibit a striking form of phenotypic plasticity. We also characterized orthologs of these genes in four species of frogs that had diverged from the two plastic species before the plasticity evolved. We found that the faster evolutionary rates of biased genes predated the evolution of the plasticity. Furthermore, biased genes showed greater expression variance than did unbiased genes, suggesting that they may be more dispensable. Phenotypic plasticity may therefore evolve when dispensable genes are co-opted for novel function in environmentally induced phenotypes. Thus, relaxed genetic constraint may be a cause--not a consequence--of the evolution of phenotypic plasticity, and thereby contribute to the evolution of novel traits.
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Insects with facultative social behaviour permit direct examination of factors associated with the expression of division of labour: why do some females remain in their natal nest as nonreproductive foragers, while others disperse? The facultatively social halictid bee Megalopta genalis shows strong reproductive division of labour, associated with body size (foragers tend to be smaller than queens and dispersers). We used M. genalis to test two hypotheses for the expression of worker behaviour: (1) queens suppress reproduction by subordinates, which then forage, and (2) small-bodied females are handicapped as reproductives, and therefore take on a foraging role to assist a more fertile relative (the ‘subfertility’ hypothesis). We removed queens from 19 nests and found that the remaining foragers enlarged their ovaries and reproduced at the same rate as solitary reproductives from unmanipulated (nonremoval) nests. This observation suggests that queen dominance limited reproduction by subordinates, and that foragers were not handicapped reproductives. To investigate the effect of body size variation on reproductive rate in the absence of social interactions, we placed single, newly eclosed females into 31 observation nests. Body size was not correlated with reproductive output or with the females' tenure in the observation nests. Nor was there any correlation between body size and number of brood cells in 21 solitary-female nonremoval nests. Taken together these data show that small females were not inherently poor reproductives. We also found that ovaries of reproductive females from social groups were larger than those of solitary reproductives, suggesting that social structure shapes ovary development.
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Phenotypic plasticity has long been suspected to allow invasive species to expand their geographic range across large-scale environmental gradients. We tested this possibility in Australia using a continental scale survey of the invasive tree Parkinsonia aculeata (Fabaceae) in twenty-three sites distributed across four climate regions and three habitat types. Using tree-level responses, we detected a trade-off between seed mass and seed number across the moisture gradient. Individual trees plastically and reversibly produced many small seeds at dry sites or years, and few big seeds at wet sites and years. Bigger seeds were positively correlated with higher seed and seedling survival rates. The trade-off, the relation between seed mass, seed and seedling survival, and other fitness components of the plant life-cycle were integrated within a matrix population model. The model confirms that the plastic response resulted in average fitness benefits across the life-cycle. Plasticity resulted in average fitness being positively maintained at the wet and dry range margins where extinction risks would otherwise have been high ("Jack-of-all-Trades" strategy JT), and fitness being maximized at the species range centre where extinction risks were already low ("Master-of-Some" strategy MS). The resulting hybrid "Jack-and-Master" strategy (JM) broadened the geographic range and amplified average fitness in the range centre. Our study provides the first empirical evidence for a JM species. It also confirms mechanistically the importance of phenotypic plasticity in determining the size, the shape and the dynamic of a species distribution. The JM allows rapid and reversible phenotypic responses to new or changing moisture conditions at different scales, providing the species with definite advantages over genetic adaptation when invading diverse and variable environments. Furthermore, natural selection pressure acting on phenotypic plasticity is predicted to result in maintenance of the JT and strengthening of the MS, further enhancing the species invasiveness in its range centre.
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A flexible statistical framework is developed for the analysis of read counts from RNA-Seq gene expression studies. It provides the ability to analyse complex experiments involving multiple treatment conditions and blocking variables while still taking full account of biological variation. Biological variation between RNA samples is estimated separately from the technical variation associated with sequencing technologies. Novel empirical Bayes methods allow each gene to have its own specific variability, even when there are relatively few biological replicates from which to estimate such variability. The pipeline is implemented in the edgeR package of the Bioconductor project. A case study analysis of carcinoma data demonstrates the ability of generalized linear model methods (GLMs) to detect differential expression in a paired design, and even to detect tumour-specific expression changes. The case study demonstrates the need to allow for gene-specific variability, rather than assuming a common dispersion across genes or a fixed relationship between abundance and variability. Genewise dispersions de-prioritize genes with inconsistent results and allow the main analysis to focus on changes that are consistent between biological replicates. Parallel computational approaches are developed to make non-linear model fitting faster and more reliable, making the application of GLMs to genomic data more convenient and practical. Simulations demonstrate the ability of adjusted profile likelihood estimators to return accurate estimators of biological variability in complex situations. When variation is gene-specific, empirical Bayes estimators provide an advantageous compromise between the extremes of assuming common dispersion or separate genewise dispersion. The methods developed here can also be applied to count data arising from DNA-Seq applications, including ChIP-Seq for epigenetic marks and DNA methylation analyses.
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Heterogeneity and latent variables are now widely recognized as major sources of bias and variability in high-throughput experiments. The most well-known source of latent variation in genomic experiments are batch effects—when samples are processed on different days, in different groups or by different people. However, there are also a large number of other variables that may have a major impact on high-throughput measurements. Here we describe the sva package for identifying, estimating and removing unwanted sources of variation in high-throughput experiments. The sva package supports surrogate variable estimation with the sva function, direct adjustment for known batch effects with the ComBat function and adjustment for batch and latent variables in prediction problems with the fsva function. Availability: The R package sva is freely available from http://www.bioconductor.org. Contact: jleek{at}jhsph.edu Supplementary information: Supplementary data are available at Bioinformatics online.
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Understanding polyphenism, the ability of a single genome to express multiple morphologically and behaviourally distinct phenotypes, is an important goal for evolutionary and developmental biology. Polyphenism has been key to the evolution of the Hymenoptera, and particularly the social Hymenoptera where the genome of a single species regulates distinct larval stages, sexual dimorphism and physical castes within the female sex. Transcriptomic analyses of social Hymenoptera will therefore provide unique insights into how changes in gene expression underlie such complexity. Here we describe gene expression in individual specimens of the pre-adult stages, sexes and castes of the key pollinator, the buff-tailed bumblebee Bombus terrestris. cDNA was prepared from mRNA from five life cycle stages (one larva, one pupa, one male, one gyne and two workers) and a total of 1,610,742 expressed sequence tags (ESTs) were generated using Roche 454 technology, substantially increasing the sequence data available for this important species. Overlapping ESTs were assembled into 36,354 B. terrestris putative transcripts, and functionally annotated. A preliminary assessment of differences in gene expression across non-replicated specimens from the pre-adult stages, castes and sexes was performed using R-STAT analysis. Individual samples from the life cycle stages of the bumblebee differed in the expression of a wide array of genes, including genes involved in amino acid storage, metabolism, immunity and olfaction. Detailed analyses of immune and olfaction gene expression across phenotypes demonstrated how transcriptomic analyses can inform our understanding of processes central to the biology of B. terrestris and the social Hymenoptera in general. For example, examination of immunity-related genes identified high conservation of important immunity pathway components across individual specimens from the life cycle stages while olfactory-related genes exhibited differential expression with a wider repertoire of gene expression within adults, especially sexuals, in comparison to immature stages. As there is an absence of replication across the samples, the results of this study are preliminary but provide a number of candidate genes which may be related to distinct phenotypic stage expression. This comprehensive transcriptome catalogue will provide an important gene discovery resource for directed programmes in ecology, evolution and conservation of a key pollinator.
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Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts-solitary reproductive females and dispersing nest foundresses-to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.
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Worker honey bees undergo a socially regulated, highly stable lipid loss as part of their behavioral maturation. We used large-scale transcriptomic and proteomic experiments, physiological experiments and RNA interference to explore the mechanistic basis for this lipid loss. Lipid loss was associated with thousands of gene expression changes in abdominal fat bodies. Many of these genes were also regulated in young bees by nutrition during an initial period of lipid gain. Surprisingly, in older bees, which is when maximum lipid loss occurs, diet played less of a role in regulating fat body gene expression for components of evolutionarily conserved nutrition-related endocrine systems involving insulin and juvenile hormone signaling. By contrast, fat body gene expression in older bees was regulated more strongly by evolutionarily novel regulatory factors, queen mandibular pheromone (a honey bee-specific social signal) and vitellogenin (a conserved yolk protein that has evolved novel, maturation-related functions in the bee), independent of nutrition. These results demonstrate that conserved molecular pathways can be manipulated to achieve stable lipid loss through evolutionarily novel regulatory processes.
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Using brain transcriptomic profiles from 853 individual honey bees exhibiting 48 distinct behavioral phenotypes in naturalistic contexts, we report that behavior-specific neurogenomic states can be inferred from the coordinated action of transcription factors (TFs) and their predicted target genes. Unsupervised hierarchical clustering of these transcriptomic profiles showed three clusters that correspond to three ecologically important behavioral categories: aggression, maturation, and foraging. To explore the genetic influences potentially regulating these behavior-specific neurogenomic states, we reconstructed a brain transcriptional regulatory network (TRN) model. This brain TRN quantitatively predicts with high accuracy gene expression changes of more than 2,000 genes involved in behavior, even for behavioral phenotypes on which it was not trained, suggesting that there is a core set of TFs that regulates behavior-specific gene expression in the bee brain, and other TFs more specific to particular categories. TFs playing key roles in the TRN include well-known regulators of neural and behavioral plasticity, e.g., Creb, as well as TFs better known in other biological contexts, e.g., NF-κB (immunity). Our results reveal three insights concerning the relationship between genes and behavior. First, distinct behaviors are subserved by distinct neurogenomic states in the brain. Second, the neurogenomic states underlying different behaviors rely upon both shared and distinct transcriptional modules. Third, despite the complexity of the brain, simple linear relationships between TFs and their putative target genes are a surprisingly prominent feature of the networks underlying behavior.
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Phenotypic plasticity allows organisms to produce alternative phenotypes under different conditions and represents one of the most important ways by which organisms adaptively respond to the environment. However, the relationship between phenotypic plasticity and molecular evolution remains poorly understood. We addressed this issue by investigating the evolution of genes associated with phenotypically plastic castes, sexes, and developmental stages of the fire ant Solenopsis invicta. We first determined if genes associated with phenotypic plasticity in S. invicta evolved at a rapid rate, as predicted under theoretical models. We found that genes differentially expressed between S. invicta castes, sexes, and developmental stages all exhibited elevated rates of evolution compared with ubiquitously expressed genes. We next investigated the evolutionary history of genes associated with the production of castes. Surprisingly, we found that orthologs of caste-biased genes in S. invicta and the social bee Apis mellifera evolved rapidly in lineages without castes. Thus, in contrast to some theoretical predictions, our results suggest that rapid rates of molecular evolution may not arise primarily as a consequence of phenotypic plasticity. Instead, genes evolving under relaxed purifying selection may more readily adopt new forms of biased expression during the evolution of alternate phenotypes. These results suggest that relaxed selective constraint on protein-coding genes is an important and underappreciated element in the evolutionary origin of phenotypic plasticity.
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Developmental maternal effects are a potentially important source of phenotypic variation, but they can be difficult to distinguish from other environmental factors. This is an important distinction within the context of social evolution, because if variation in offspring helping behavior is due to maternal manipulation, social selection may act on maternal phenotypes, as well as those of offspring. Factors correlated with social castes have been linked to variation in developmental nutrition, which might provide opportunity for females to manipulate the social behavior of their offspring. Megalopta genalis is a mass-provisioning facultatively eusocial sweat bee for which production of males and females in social and solitary nests is concurrent and asynchronous. Female offspring may become either gynes (reproductive dispersers) or workers (non-reproductive helpers). We predicted that if maternal manipulation plays a role in M. genalis caste determination, investment in daughters should vary more than for sons. The mass and protein content of pollen stores provided to female offspring varied significantly more than those of males, but volume and sugar content did not. Sugar content varied more among female eggs in social nests than in solitary nests. Provisions were larger, with higher nutrient content, for female eggs and in social nests. Adult females and males show different patterns of allometry, and their investment ratio ranged from 1.23 to 1.69. Adult body weight varied more for females than males, possibly reflecting increased variation in maternal investment in female offspring. These differences are consistent with a role for maternal manipulation in the social plasticity observed in M. genalis.
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Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.
Book
The first comprehensive synthesis on development and evolution: it applies to all aspects of development, at all levels of organization and in all organisms, taking advantage of modern findings on behavior, genetics, endocrinology, molecular biology, evolutionary theory and phylogenetics to show the connections between developmental mechanisms and evolutionary change. This book solves key problems that have impeded a definitive synthesis in the past. It uses new concepts and specific examples to show how to relate environmentally sensitive development to the genetic theory of adaptive evolution and to explain major patterns of change. In this book development includes not only embryology and the ontogeny of morphology, sometimes portrayed inadequately as governed by "regulatory genes," but also behavioral development and physiological adaptation, where plasticity is mediated by genetically complex mechanisms like hormones and learning. The book shows how the universal qualities of phenotypes--modular organization and plasticity--facilitate both integration and change. Here you will learn why it is wrong to describe organisms as genetically programmed; why environmental induction is likely to be more important in evolution than random mutation; and why it is crucial to consider both selection and developmental mechanism in explanations of adaptive evolution. This book satisfies the need for a truly general book on development, plasticity and evolution that applies to living organisms in all of their life stages and environments. Using an immense compendium of examples on many kinds of organisms, from viruses and bacteria to higher plants and animals, it shows how the phenotype is reorganized during evolution to produce novelties, and how alternative phenotypes occupy a pivotal role as a phase of evolution that fosters diversification and speeds change. The arguments of this book call for a new view of the major themes of evolutionary biology, as shown in chapters on gradualism, homology, environmental induction, speciation, radiation, macroevolution, punctuation, and the maintenance of sex. No other treatment of development and evolution since Darwin's offers such a comprehensive and critical discussion of the relevant issues. Developmental Plasticity and Evolution is designed for biologists interested in the development and evolution of behavior, life-history patterns, ecology, physiology, morphology and speciation. It will also appeal to evolutionary paleontologists, anthropologists, psychologists, and teachers of general biology.
Article
Different views of the pattern of social evolution among the highly eusocial bees have arisen as a result of discordance between past molecular and morphology-based phylogenies. Here we present new data and taxa for four molecular data sets and reassess the morphological characters available to date. We show there is no significant character incongruence between four molecular data sets (two nuclear and two mitochondrial), but highly significant character incongruence leads to topological incongruence between the molecular and morphological data. We investigate the effects of using different outgroup combinations to root the estimated tree. We also consider various ways in which biases in the sequence data could be misleading, using several maximum likelihood models, LogDet corrections, and spectral analyses. Ultimately, we concede there is strong discordance between the molecular and morphological data partitions and appropriately apply the conditional combination approach in this case. We also find two equally well supported placements of the root for the molecular trees, one supported by 16S and 28S sequences, the other supported by cytochrome b and opsin. The strength of the evidence leads us to accept two equally well supported hypotheses based on analyses of the molecular data sets. These are the most rigorously supported hypotheses of corbiculate bee relationships at this time, and frame our argument that highly eusocial behavior within the corbiculate bees evolved twice independently.
Research
Bumble bees represent a taxon with an intermediate level of eusociality within Hymenoptera. The clear division of reproduction between a single founding queen and the largely sterile workers is characteristic for highly eusocial species, whereas the morphological similarity between the bumble bee queen and the workers is typical for more primitively eusocial hymenopterans. Also, unlike other highly eusocial hymenopterans, division of labour among worker sub-castes is plastic and not predetermined by morphology or age. We conducted a differential expression analysis based on RNA-seq data from 11 combinations of developmental stage and caste to investigate how a single genome can produce the distinct castes of queens, workers and males in the buff-tailed bumble bee Bombus terrestris. Based on expression patterns, we found males to be the most distinct of all adult castes (2,411 transcripts differentially expressed compared to non-reproductive workers). However, only relatively few transcripts were differentially expressed between males and workers during development (larvae: 71, pupae: 162). This indicates the need for more distinct expression patterns to control behaviour and physiology in adults compared to those required to create different morphologies. Among female castes, reproductive workers and their non-reproductive sisters displayed differential expression in over ten times more transcripts compared to the differential expression found between reproductive workers and their mother queen. This suggests a strong shift towards a more queen-like behaviour and physiology when a worker becomes fertile. This contrasts with eusocial species where reproductive workers are more similar to non-reproductive workers than the queen. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Article
Agriculture arose during a period of profound global climatic and ecological change following the end of the Pleistocene. Yet, the role of phenotypic plasticity – an organism's ability to change its phenotype in response to the environment – and environmental influences in the dramatic phenotypic transformations that occurred during plant domestication are poorly understood. Another factor possibly influential in agricultural origins, the productivity of crop plant wild progenitors in Late Pleistocene vs. Holocene environments, has received increasing attention recently and merits further investigation. In this study, we examined phenotypic characteristics and productivity (biomass, seed yield) in the wild progenitor of maize, the teosinte Zea mays ssp. parviglumis H.H. Iltis & Doebley, when it was first exploited and cultivated by growing it in atmospheric CO2 concentrations and temperatures characteristic of the late-glacial and early Holocene periods. Plants responded with a number of attributes uncharacteristic of teosinte in today's environments, including maize-type traits in vegetative architecture, inflorescence sexuality, and seed maturation. Teosinte productivity was significantly lower in late-glacial compared with early Holocene and modern environments. Our evidence indicates that: a) ancestral biological characteristics of crop plant progenitors aren't always predicted from living examples, b) some important maize phenotypic traits were present at initial human exploitation and selection, and c) Pleistocene plant productivity should be considered a significant factor in the chronology of food production origins.
Article
Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood-tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood-tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood-tenders and foragers (~300 genes). The expression profile of fertile workers is more worker-like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.
Article
Vitellogenin (Vg) is best known as a yolk protein precursor. Vg also functions to regulate behavioural maturation in adult honey bee workers, but the underlying molecular mechanisms by which it exerts this novel effect are largely unknown. We used abdominal vitellogenin (vg) knockdown with RNA interference (RNAi) and brain transcriptomic profiling to gain insights into how Vg influences honey bee behavioural maturation. We found that vg knockdown caused extensive gene expression changes in the bee brain, with much of this transcriptional response involving changes in central biological functions such as energy metabolism. vg knockdown targeted many of the same genes that show natural, maturation-related differences, but the direction of change for the genes in these two contrasts was not correlated. By contrast, vg knockdown targeted many of the same genes that are regulated by juvenile hormone (JH) and there was a significant correlation for the direction of change for the genes in these two contrasts. These results indicate that the tight coregulatory relationship that exists between JH and Vg in the regulation of honey bee behavioural maturation is manifest at the genomic level and suggest that these two physiological factors act through common pathways to regulate brain gene expression and behaviour.
Article
We compare the behaviour of daughters of Evylaeus albipes females from eusocial populations from the West of France with those from a non-eusocial population from the East of the country. When non-eusocial population females are placed in the laboratory under day lengths and temperature conditions similar to those experienced by eusocial foundresses under natural conditions, all five produced a brood of males and overwintering daughters with no workers. When 18 nests were initiated by non-eusocial foundresses under short summer daylengths but warmer than normal temperatures, two produced one worker amongst overwintering female and male brood. Both worker-producing non-eusocial females were from the warmest of the eastern localities. When foundresses of the social population are placed under day length conditions typical for the noneusocial population but with temperature conditions that are intermediate between the two, all five produced at least one worker. Similarly, if the first brood produced by social foundresses is removed, they raise another brood that contains workers whereas non-eusocial population foundresses who have their first brood removed produce a second brood of overwintering females (although one foundress, again from the warmest of the non-eusocial localities, produced one worker in each of two broods, also with males and overwintering females). We conclude that i) non-eusocial foundresses do not readily produce workers under long summer conditions; ii) the lack of worker production by most non-eusocial population females is not because they cannot produce two broods, but because they have a tendency not to produce workers; iii) eusocial population daughters will become active without diapausing in the presence of any other female ‐ even of the closely related E. calceatus, unless the first individual to eclose is the smallest and iv) social population foundresses are incapable of producing over
Article
Augochlorella striata was studied at the northern limit of its range. The study population contained a mixture of solitary and social nest foundresses. Eusocial foundresses produced 1 or 2 workers before switching to a male biased brood. Solitary foundresses produced males first. Cells vacated by eclosed offspring were reused late in summer. A female biased brood resulted from cell reuse in both solitary and eusocial nests. Workers were slightly smaller than their mothers and were sterile although most of them mated. In comparison to published data from a Kansas population of this species, the Nova Scotia population had i) a lower proportion of multiple foundress nests, ii) a smaller worker brood and iii) a briefer period of foraging activity but iv) comparable overall nest productivity.
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Exchange of liquid food among adults (trophallaxis) is documented for the first time in New World sweat bees (Halictinae). Megalopta genalis and M. ecuadoria are facultatively social, and in social groups foragers regularly give food to the oldest resident female bee, which dominates social interactions. In turn, the oldest resident sometimes re-distributes this food, and shares it with younger foragers. Food is sometimes offered freely, but often the dominant bee exhibits escalating aggressive behavior until she is fed, whereupon she immediately ceases to be aggressive. The occurrence of trophallaxis in a species with mass-provisioned larvae provides an opportunity to examine the ritualization of social behavior. Trophallaxis also increases survivorship of males and females by almost 50% under experimental conditions, suggesting the behavior is also important in ecological contexts.
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In the subalpine region of the Rocky Mountains of Colorado, United States, Halictus rubicundus has a solitary life cycle, but it is social in other parts of its known range. The brood is protandrous, with a nearly equal investment in the sexes. Productivity averages 6.5 offspring per foundress female, similar to the second brood of social nests in New York, but less than the combined productivity of both New York broods. Leucophora sp. (Diptera: Anthomyiidae) is the principal cause of brood mortality in Colorado. Foundress females in about half the nests survive until brood emerge as adults. Retention of these foundresses decreases offspring mortality by 68%. Comparable abilities to express solitary behavior with a single brood may characterize other eusocial halictine lineages that have successfully invaded high altitudes in the Rocky Mountains. The apparent inability to do this may help explain the absence of other eusocial halictine bees and polistine wasps at high altitudes, despite their success at lower elevations in the same mountains. Presence or absence of this ability may help explain latitudinal distributions of these lineages in North America. Holarctic distributions of lineages with eusocial behavior can be explained by migration as solitary populations from Eurasia to North America across Pleistocene Bering land bridges, with re-expression of double-brooded, eusocial behavior when the species then extended their ranges southward in North America.
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1. A wild Edinburgh strain of D. melanogaster produced no flies showing a break in the posterior crossvein when bred at 25⚬ C., but a certain number occurred (as phenocopies) when the pupae aged 21-23 hours were subjected to 40⚬ C. for four hours. 2. Selection was practised for and against the appearance of the phenocopy, and rapid progress occurred in both directions. After about 14 generations of selection, some flies in the upward selected strain were found to show the effect even when not exposed to the heat shock. From these, lines were built up which threw a high proportion of crossveinless individuals when kept continuously at 25⚬ C. (and even more at 18⚬ C.). 3. The crossveinless character, originally a typical 'acquired character,' has become incorporated into the genetic make up of the selected races. A process of 'genetic assimilation' is described by which this might be supposed to happen; it depends on the tendency of selection not merely to increase the frequency of any favorable character, but also to stabilise its development. A similar suggestion has been advanced by Schmalhausen (1947). 4. The genetic basis of the assimilated crossveinless character is polygenic. There is little evidence of any definite distinction between canalising and switch genes.