RESUMEN
Variation in endocrine signaling is proposed to underlie the evolution and regulation of social life histories, but the genetic architecture of endocrine signaling is still poorly understood. An excellent example of a hormonally influenced set of social traits is found in the honey bee (Apis mellifera): a dynamic and mutually suppressive relationship between juvenile hormone (JH) and the yolk precursor protein vitellogenin (Vg) regulates behavioral maturation and foraging of workers. Several other traits cosegregate with these behavioral phenotypes, comprising the pollen hoarding syndrome (PHS) one of the best-described animal behavioral syndromes. Genotype differences in responsiveness of JH to Vg are a potential mechanistic basis for the PHS. Here, we reduced Vg expression via RNA interference in progeny from a backcross between 2 selected lines of honey bees that differ in JH responsiveness to Vg reduction and measured JH response and ovary size, which represents another key aspect of the PHS. Genetic mapping based on restriction site-associated DNA tag sequencing identified suggestive quantitative trait loci (QTL) for ovary size and JH responsiveness. We confirmed genetic effects on both traits near many QTL that had been identified previously for their effect on various PHS traits. Thus, our results support a role for endocrine control of complex traits at a genetic level. Furthermore, this first example of a genetic map of a hormonal response to gene knockdown in a social insect helps to refine the genetic understanding of complex behaviors and the physiology that may underlie behavioral control in general.
Asunto(s)
Abejas/fisiología , Conducta Animal/fisiología , Técnicas de Silenciamiento del Gen , Hormonas Juveniles/fisiología , Vitelogeninas/fisiología , Animales , Abejas/genética , Cruzamientos Genéticos , Femenino , Genotipo , Tamaño de los Órganos , Ovario/fisiología , Fenotipo , Polimorfismo de Nucleótido Simple , Sitios de Carácter Cuantitativo , Análisis de Secuencia de ADNRESUMEN
Honey bee workers display remarkable flexibility in the aging process. This plasticity is closely tied to behavioral maturation. Workers who initiate foraging behavior at earlier ages have shorter lifespans, and much of the variation in total lifespan can be explained by differences in pre-foraging lifespan. Vitellogenin (Vg), a yolk precursor protein, influences worker lifespan both as a regulator of behavioral maturation and through anti-oxidant and immune functions. Experimental reduction of Vg mRNA, and thus Vg protein levels, in wild-type bees results in precocious foraging behavior, decreased lifespan, and increased susceptibility to oxidative damage. We sought to separate the effects of Vg on lifespan due to behavioral maturation from those due to immune and antioxidant function using two selected strains of honey bees that differ in their phenotypic responsiveness to Vg gene knockdown. Surprisingly, we found that lifespans lengthen in the strain described as behaviorally and hormonally insensitive to Vg reduction. We then performed targeted gene expression analyses on genes hypothesized to mediate aging and lifespan: the insulin-like peptides (Ilp1 and 2) and manganese superoxide dismutase (mnSOD). The two honey bee Ilps are the most upstream components in the insulin-signaling pathway, which influences lifespan in Drosophila melanogaster and other organisms, while manganese superoxide dismutase encodes an enzyme with antioxidant functions in animals. We found expression differences in the llps in fat body related to behavior (llp1 and 2) and genetic background (Ilp2), but did not find strain by treatment effects. Expression of mnSOD was also affected by behavior and genetic background. Additionally, we observed a differential response to Vg knockdown in fat body expression of mnSOD, suggesting that antioxidant pathways may partially explain the strain-specific lifespan responses to Vg knockdown.
Asunto(s)
Abejas/fisiología , Longevidad , Vitelogeninas/fisiología , Tejido Adiposo/metabolismo , Animales , Encéfalo/metabolismo , Técnicas de Silenciamiento del Gen , Genotipo , Proteínas de Insectos/fisiología , Especificidad de la Especie , Superóxido Dismutasa/fisiología , Vitelogeninas/genéticaRESUMEN
Some genes regulate phenotypes that are either present or absent. They are often important regulators of developmental switches and are involved in morphological evolution. We have little understanding of the molecular mechanisms by which these absence/presence gene functions have evolved, because the phenotype and fitness of molecular intermediate forms are unknown. Here, we studied the sex-determining switch of 14 natural sequence variants of the csd gene among 76 genotypes of the honeybee (Apis mellifera). Heterozygous genotypes (different specificities) of the csd gene determine femaleness, while hemizygous genotypes (single specificity) determine maleness. Homozygous genotypes of the csd gene (same specificity) are lethal. We found that at least five amino acid differences and length variation between Csd specificities in the specifying domain (PSD) were sufficient to regularly induce femaleness. We estimated that, on average, six pairwise amino acid differences evolved under positive selection. We also identified a natural evolutionary intermediate that showed only three amino acid length differences in the PSD relative to its parental allele. This genotype showed an intermediate fitness because it implemented lethality regularly and induced femaleness infrequently (i.e., incomplete penetrance). We suggest incomplete penetrance as a mechanism through which new molecular switches can gradually and adaptively evolve.
Asunto(s)
Abejas/genética , Evolución Molecular , Proteínas de Insectos/genética , Procesos de Determinación del Sexo , Secuencia de Aminoácidos , Animales , Abejas/crecimiento & desarrollo , Femenino , Variación Genética , Genotipo , Proteínas de Insectos/química , Masculino , Datos de Secuencia Molecular , Alineación de SecuenciaRESUMEN
Honey bee workers exhibit an age-based division of labor (temporal polyethism, DOL). Younger bees transition through sets of tasks within the nest; older bees forage outside. Components of temporal polyethism remain unrevealed. Here, we investigate the timing and pattern of pre-foraging behavior in distinct strains of bees to (1) determine if a general pattern of temporal DOL exists in honey bees, (2) to demonstrate a direct genetic impact on temporal pacing, and (3) to further elucidate the mechanisms controlling foraging initiation. Honey bees selected for differences in stored pollen demonstrate consistent differences in foraging initiation age. Those selected for increased pollen storage (high pollen hoarding strain, HSBs) initiate foraging earlier in life than those selected for decreased pollen storage (low pollen hoarding strain, LSBs). We found that HSBs both initiate and terminate individual pre-foraging tasks earlier than LSBs when housed in a common hive environment. Unselected commercial bees (wild type) generally demonstrated intermediate behavioral timing. There were few differences between genotypes for the proportion of pre-foraging effort dedicated to individual tasks, though total pre-foraging effort differences differed dramatically. This demonstrates that behavioral pacing can be accelerated or slowed, but the pattern of behavior is not fundamentally altered, suggesting a general pattern of temporal behavior in honey bees. This also demonstrates direct genetic control of temporal pacing. Finally, our results suggest that earlier HSB protein (pollen) consumption termination compared to LSBs may contribute to an earlier decline in hemolymph vitellogenin protein titers, which would explain their earlier onset of foraging.
RESUMEN
The pollen hoarding syndrome consists of a large suite of correlated traits in honey bees that may have played an important role in colony organization and consequently the social evolution of honey bees. The syndrome was first discovered in two strains that have been artificially selected for high and low pollen hoarding. These selected strains are used here to further investigate the phenotypic and genetic links between two central aspects of the pollen hoarding syndrome, sucrose responsiveness and pollen hoarding. Sons of hybrid queen offspring of these two strains were tested for sucrose responsiveness and used to produce colonies with either a highly responsive or an unresponsive father. These two colony groups differed significantly in the amount of pollen stored on brood combs and with regards to their relationship between brood and pollen amounts. Additionally, four quantitative trait loci (QTL) for pollen hoarding behavior were assessed for their effect on sucrose responsiveness. Drone offspring of two hybrid queens were phenotyped for responsiveness and genotyped at marker loci for these QTL, identifying some pleiotropic effects of the QTL with significant QTL interactions. Both experiments thus provided corroborating evidence that the distinct traits of the pollen hoarding syndrome are mechanistically and genetically linked, and that these links are complex and dependent on background genotype. The study demonstrates genetic worker-drone correlations within the context of the pollen hoarding syndrome and establishes that an indirect selection response connects pollen hoarding and sucrose responsiveness, regardless of which trait is directly selected.
RESUMEN
Nutrient sensitive insulin-like peptides (ILPs) have profound effects on invertebrate metabolism, nutrient storage, fertility and aging. Many insects transcribe ILPs in specialized neurosecretory cells at changing levels correlated with life history. However, the major site of insect metabolism and nutrient storage is not the brain, but rather the fat body, where functions of ILP expression are rarely studied and poorly understood. Fat body is analogous to mammalian liver and adipose tissue, with nutrient stores that often correlate with behavior. We used the honey bee (Apis mellifera), an insect with complex behavior, to test whether ILP genes in fat body respond to experimentally induced changes of behavioral physiology. Honey bee fat body influences endocrine state and behavior by secreting the yolk protein precursor vitellogenin (Vg), which suppresses lipophilic juvenile hormone and social foraging behavior. In a two-factorial experiment, we used RNA interference (RNAi)-mediated vg gene knockdown and amino acid nutrient enrichment of hemolymph (blood) to perturb this regulatory module. We document factor-specific changes in fat body ilp1 and ilp2 mRNA, the bee's ILP-encoding genes, and confirm that our protocol affects social behavior. We show that ilp1 and ilp2 are regulated independently and differently and diverge in their specific expression-localization between fat body oenocyte and trophocyte cells. Insect ilp functions may be better understood by broadening research to account for expression in fat body and not only brain.
Asunto(s)
Abejas/genética , Abejas/fisiología , Conducta Animal/fisiología , Cuerpo Adiposo/metabolismo , Genes de Insecto/genética , Insulina/genética , Conducta Social , Albúminas/metabolismo , Aminoácidos/farmacología , Animales , Abejas/efectos de los fármacos , Conducta Animal/efectos de los fármacos , Cuerpo Adiposo/citología , Cuerpo Adiposo/efectos de los fármacos , Técnica del Anticuerpo Fluorescente , Regulación de la Expresión Génica/efectos de los fármacos , Hemolinfa/efectos de los fármacos , Hemolinfa/metabolismo , Miel , Insulina/metabolismo , Hormonas Juveniles/metabolismo , Modelos Biológicos , ARN Mensajero/genética , ARN Mensajero/metabolismo , Reproducibilidad de los Resultados , Volumetría , Vitelogeninas/genética , Vitelogeninas/metabolismoRESUMEN
Behavior is a quantitative trait determined by multiple genes. Some of these genes may have effects from early development and onward by influencing hormonal systems that are active during different life-stages leading to complex associations, or suites, of traits. Honey bees (Apis mellifera) have been used extensively in experiments on the genetic and hormonal control of complex social behavior, but the relationships between their early developmental processes and adult behavioral variation are not well understood. Bidirectional selective breeding on social food-storage behavior produced two honey bee strains, each with several sublines, that differ in an associated suite of anatomical, physiological, and behavioral traits found in unselected wild type bees. Using these genotypes, we document strain-specific changes during larval, pupal, and early adult life-stages for the central insect hormones juvenile hormone (JH) and ecdysteroids. Strain differences correlate with variation in female reproductive anatomy (ovary size), which can be influenced by JH during development, and with secretion rates of ecdysteroid from the ovaries of adults. Ovary size was previously assigned to the suite of traits of honey bee food-storage behavior. Our findings support that bidirectional selection on honey bee social behavior acted on pleiotropic gene networks. These networks may bias a bee's adult phenotype by endocrine effects on early developmental processes that regulate variation in reproductive traits.
Asunto(s)
Abejas/fisiología , Conducta Animal , Conducta Social , Animales , Abejas/genética , Abejas/metabolismo , Ecdisteroides/metabolismo , Femenino , Genotipo , Hormonas Juveniles/metabolismo , Larva/genética , Larva/metabolismo , Larva/fisiología , Ovario/metabolismo , Pupa/genética , Pupa/metabolismo , Pupa/fisiología , Selección Genética , Vitelogeninas/metabolismoRESUMEN
In honeybee colonies, food collection is performed by a group of mostly sterile females called workers. After an initial nest phase, workers begin foraging for nectar and pollen, but tend to bias their collection towards one or the other. The foraging choice of honeybees is influenced by vitellogenin (vg), an egg-yolk precursor protein that is expressed although workers typically do not lay eggs. The forager reproductive ground plan hypothesis (RGPH) proposes an evolutionary path in which the behavioural bias toward collecting nectar or pollen on foraging trips is influenced by variation in reproductive physiology, such as hormone levels and vg gene expression. Recently, the connections between vg and foraging behaviour were challenged by Oldroyd and Beekman (2008), who concluded from their study that the ovary, and especially vg, played no role in foraging behaviour of bees. We address their challenge directly by manipulating vg expression by RNA interference- (RNAi) mediated gene knockdown in two honeybee genotypes with different foraging behaviour and reproductive physiology. We show that the effect of vg on the food-loading decisions of the workers occurs only in the genotype where timing of foraging onset (by age) is also sensitive to vg levels. In the second genotype, changing vg levels do not affect foraging onset or bias. The effect of vg on workers' age at foraging onset is explained by the well-supported double repressor hypothesis (DHR), which describes a mutually inhibitory relationship between vg and juvenile hormone (JH) - an endocrine factor that influences development, reproduction, and behaviour in many insects. These results support the RGPH and demonstrate how it intersects with an established mechanism of honeybee behavioural control.
RESUMEN
The genetic basis of division of labor in social insects is a central question in evolutionary and behavioral biology. The honey bee is a model for studying evolutionary behavioral genetics because of its well characterized age-correlated division of labor. After an initial period of within-nest tasks, 2-3 week-old worker bees begin foraging outside the nest. Individuals often specialize by biasing their foraging efforts toward collecting pollen or nectar. Efforts to explain the origins of foraging specialization suggest that division of labor between nectar and pollen foraging specialists is influenced by genes with effects on reproductive physiology. Quantitative trait loci (QTL) mapping of foraging behavior also reveals candidate genes for reproductive traits. Here, we address the linkage of reproductive anatomy to behavior, using backcross QTL analysis, behavioral and anatomical phenotyping, candidate gene expression studies, and backcross confirmation of gene-to-anatomical trait associations. Our data show for the first time that the activity of two positional candidate genes for behavior, PDK1 and HR46, have direct genetic relationships to ovary size, a central reproductive trait that correlates with the nectar and pollen foraging bias of workers. These findings implicate two genes that were not known previously to influence complex social behavior. Also, they outline how selection may have acted on gene networks that affect reproductive resource allocation and behavior to facilitate the evolution of social foraging in honey bees.
Asunto(s)
Abejas/fisiología , Genes de Insecto , Ovario/metabolismo , Conducta Social , Animales , Femenino , Sitios de Carácter Cuantitativo , Reproducción/genéticaRESUMEN
Long-lived honey bees (Apis mellifera) develop in fall. This pattern may be explained by reduced nurse loads. When the amount of brood in colonies declines as a function of adverse foraging conditions, adult bees build up surplus nutrient stores that include vitellogenin, a behavioral affector protein that also can increase lifespan. Although the seasonal reduction in exposure to nursing tasks predictably results in vitellogenin accumulation, the assumption that long-lived adults thereby develop is confounded by a concomitant decline in foraging effort. Foraging activity reduces lifespan, and is influenced by colony resource consumption, brood pheromones, availability of nectar and pollen, and weather. Here, we perform the first controlled experiment where the nursing environment of pre-foraging sister bees was set to vary, while their foraging environment later was set to be the same. We measure vitellogenin, age at foraging onset and lifespan. We establish that reduced brood-rearing increases vitellogenin levels, and delays foraging onset and death. Longevity is largely explained by the effect of nursing on the onset of foraging behavior, but is also influenced by the level of brood-rearing independent of behavioral change. Our findings are consistent with the roles of vitellogenin in regulation of honey bee behavior and lifespan.
Asunto(s)
Longevidad/fisiología , Vitelogeninas/metabolismo , Análisis de Varianza , Animales , Abejas , Estaciones del Año , Conducta SocialRESUMEN
Variation in endocrine pathways can be a major mechanism underlying life-history evolution. Yet it is unclear whether this insight, derived primarily from solitary species, explains the origins of complex life-history traits in highly social taxa. Thus, we here document and study variation in social life-history syndromes of female fecundity, behavior, and life span in selectively bred honeybee (Apis mellifera) strains. Associated variation in endocrine signaling was uncovered by RNA interference (RNAi) silencing of the juvenile hormone (JH) suppressor gene vitellogenin. High versus low endocrine reactivity in response to vitellogenin knockdown consistently correlated with rapid social behavioral ontogeny and short life span versus slow social behavioral ontogeny and long life span. Variation in JH reactivity, furthermore, was a function of variation in fecundity (ovary size and follicle development). A JH-mediated pleiotropy of female life-history traits, including fecundity, behavior, and life span, characterizes the distantly related solitary insect Drosophila. For the first time, we document a similar regulatory principle in a highly social species where most females are alloparental helpers (workers) that seldom reproduce. We conclude that variation in endocrine pathways of solitary origin can underlie variation and evolvability of complex social life-history traits.
Asunto(s)
Abejas/metabolismo , Variación Genética , Hormonas Juveniles/metabolismo , Transducción de Señal , Conducta Social , Animales , Abejas/genética , Abejas/fisiología , Sistema Endocrino/fisiología , Retroalimentación Fisiológica , Femenino , Fertilidad , Genotipo , Longevidad , Modelos Biológicos , Ovario/fisiología , Interferencia de ARN , Vitelogeninas/genética , Vitelogeninas/metabolismoRESUMEN
Life expectancy of honey bees (Apis mellifera L.) is of general interest to gerontological research because its variability among different groups of bees is one of the most striking cases of natural plasticity of aging. Worker honey bees spend their first days of adult life working in the nest, then transition to foraging and die between 4 and 8 weeks of age. Foraging is believed to be primarily responsible for the early death of workers. Three large-scale experiments were performed to quantitatively assess the importance of flight activity, chronological age, extrinsic mortality factors and foraging specialization. Forager mortality was higher than in-hive bee mortality. Most importantly however, reducing the external mortality hazards and foraging activity did not lead to the expected strong extension of life. Most of the experimental effects were attributable to an earlier transition from hive tasks to foraging. This transition is accompanied by a significant mortality peak. The age at the onset of foraging is the central variable in worker life-history and behavioral state was found more important than chronological age for honey bee aging. However, mortality risk increased with age and the negative relation between pre-foraging and foraging lifespan indicate some senescence irrespective of behavioral state. Overall, honey bee workers exhibit a logistic mortality dynamic which is mainly caused by the age-dependent transition from a low mortality pre-foraging state to a higher mortality foraging state.
Asunto(s)
Envejecimiento/fisiología , Abejas/fisiología , Estadios del Ciclo de Vida/fisiología , Esperanza de Vida , Animales , Conducta Apetitiva/fisiología , Abejas/crecimiento & desarrollo , Vuelo Animal/fisiología , Análisis de SupervivenciaRESUMEN
BACKGROUND: Honey bees (Apis mellifera) provide a principal example of diphenic development. Excess feeding of female larvae results in queens (large reproductives). Moderate diet yields workers (small helpers). The signaling pathway that links provisioning to female developmental fate is not understood, yet we reasoned that it could include TOR (target of rapamycin), a nutrient- and energy-sensing kinase that controls organismal growth. METHODOLOGY/PRINCIPAL FINDINGS: Here, the role of Apis mellifera TOR (amTOR) in caste determination is examined by rapamycin/FK506 pharmacology and RNA interference (RNAi) gene knockdown. We show that in queen-destined larvae, the TOR inhibitor rapamycin induces the development of worker characters that are blocked by the antagonist FK506. Further, queen fate is associated with elevated activity of the Apis mellifera TOR encoding gene, amTOR, and amTOR gene knockdown blocks queen fate and results in individuals with worker morphology. CONCLUSIONS/SIGNIFICANCE: A much-studied insect dimorphism, thereby, can be governed by the TOR pathway. Our results present the first evidence for a role of TOR in diphenic development, and suggest that adoption of this ancestral nutrient-sensing cascade is one evolutionary pathway for morphological caste differentiation in social insects.
Asunto(s)
Abejas/fisiología , Conducta Animal/fisiología , Jerarquia Social , Péptidos y Proteínas de Señalización Intracelular/metabolismo , Proteínas Serina-Treonina Quinasas/metabolismo , Animales , Femenino , Regulación del Desarrollo de la Expresión Génica , Péptidos y Proteínas de Señalización Intracelular/antagonistas & inhibidores , Péptidos y Proteínas de Señalización Intracelular/genética , Larva/crecimiento & desarrollo , Larva/metabolismo , Proteínas Serina-Treonina Quinasas/antagonistas & inhibidores , Proteínas Serina-Treonina Quinasas/genética , ARN Interferente Pequeño/farmacología , Sirolimus/farmacología , Serina-Treonina Quinasas TORRESUMEN
Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.
Asunto(s)
Abejas/fisiología , Conducta Social , Vitelogeninas/genética , Animales , Conducta AlimentariaRESUMEN
The honeybee has been the most important insect species for study of social behavior. The recently released draft genomic sequence for the bee will accelerate honeybee behavioral genetics. Although we lack sufficient tools to manipulate this genome easily, quantitative trait loci (QTLs) that influence natural variation in behavior have been identified and tested for their effects on correlated behavioral traits. We review what is known about the genetics and physiology of two behavioral traits in honeybees, foraging specialization (pollen versus nectar), and defensive behavior, and present evidence that map-based cloning of genes is more feasible in the bee than in other metazoans. We also present bioinformatic analyses of candidate genes within QTL confidence intervals (CIs). The high recombination rate of the bee made it possible to narrow the search to regions containing only 17-61 predicted peptides for each QTL, although CIs covered large genetic distances. Knowledge of correlated behavioral traits, comparative bioinformatics, and expression assays facilitated evaluation of candidate genes. An overrepresentation of genes involved in ovarian development and insulin-like signaling components within pollen foraging QTL regions suggests that an ancestral reproductive gene network was co-opted during the evolution of foraging specialization. The major QTL influencing defensive/aggressive behavior contains orthologs of genes involved in central nervous system activity and neurogenesis. Candidates at the other two defensive-behavior QTLs include modulators of sensory signaling (Am5HT(7) serotonin receptor, AmArr4 arrestin, and GABA-B-R1 receptor). These studies are the first step in linking natural variation in honeybee social behavior to the identification of underlying genes.
Asunto(s)
Abejas/genética , Conducta Alimentaria/fisiología , Genética Conductual , Genoma , Comportamiento de Nidificación/fisiología , Animales , Abejas/fisiología , Mapeo Cromosómico , Clonación Molecular , Sitios de Carácter CuantitativoRESUMEN
A fundamental goal of sociobiology is to explain how complex social behaviour evolves, especially in social insects, the exemplars of social living. Although still the subject of much controversy, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes to result in sib-care, the hallmark of highly evolved social life in insects. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.
Asunto(s)
Abejas/fisiología , Evolución Biológica , Conducta Alimentaria/fisiología , Conducta Materna/fisiología , Reproducción/fisiología , Conducta Social , Envejecimiento/fisiología , Animales , Femenino , Infertilidad Femenina , Ovario/fisiología , Polen/metabolismoRESUMEN
One of the best examples of a natural behavioral syndrome is the pollen-hoarding syndrome in honeybees that ties together multiple behavioral phenotypes, ranging from foraging behavior to behavioral ontogeny and learning performance. A central behavioral factor is the bees' responsiveness to sucrose, measured as their proboscis extension reflex. This study examines the genetics of this trait in diploid worker and haploid male honeybees (drones) to learn more about the genetic architecture of the overall behavioral syndrome, using original strains selected for pollen-hoarding behavior. We show that a significant proportion of the phenotypic variability is determined by genotype in males and workers. Second, our data present overwhelming evidence for pleiotropic effects of previously identified quantitative trait loci for foraging behavior (pln-QTL) and epistatic interactions among them. Furthermore, we report on three genomic QTL scans (two reciprocal worker backcrosses and one drone hybrid population) derived from our selection strains. We present at least one significant and two putative new QTL directly affecting the sucrose response of honeybees. Thus, this study demonstrates the modular genetic architecture of behavioral syndromes in general, and elucidates the genetic architecture of the pollen-hoarding behavioral syndrome in particular. Understanding this behavioral syndrome is important for understanding the division of labor in social insects and social evolution itself.
Asunto(s)
Abejas/efectos de los fármacos , Abejas/genética , Conducta Animal/fisiología , Actividad Motora/fisiología , Sitios de Carácter Cuantitativo/genética , Sacarosa/farmacología , Animales , Abejas/crecimiento & desarrollo , Cruzamientos Genéticos , Diploidia , Femenino , Haploidia , Masculino , Actividad Motora/genética , Fenotipo , PolenRESUMEN
Division of labour in social insect colonies relies on behavioural functional differentiation (specialization) of individuals with similar genomes. However, individual behavioural traits do not evolve independently of each other (behavioural syndromes). A prime example is the suite of behavioural differences in honeybee workers that has evolved in response to bidirectional selection on pollen hoarding of honeybee colonies (pollen-hoarding syndrome). More generally, these differences reflect functional differentiation between nectar and pollen foragers. We demonstrate here that this pollen-hoarding syndrome extends to drones. Similar to what has been shown in workers, drones from the high-pollen-hoarding strain had a higher locomotion activity after emergence, and they initiated flight earlier than did males derived from the low-pollen-hoarding strain, with hybrids intermediate. However, these two behavioural traits were unlinked at the individual level. We also found that social environment (the colony) affects the age at which drones initiate flight. The indirect selection responses of male behaviour suggest that male and worker evolution are not independent and may constrain each other's evolution. Furthermore, we identified three distinct peaks in the probability of flight initiation over the course of the experiment and a decreased phenotypic variability in the 'hybrid' males, contrary to quantitative genetic expectations.
RESUMEN
Biodemographic studies of insects have significantly enhanced our understanding of the biology of aging. Eusocial insects have evolved to form different groups of colony members that are specialized for particular tasks and highly dependent on each other. These different groups (castes and sexes) also differ strongly in their life expectancy but relatively little is known about their mortality dynamics. In this study we present data on the age-specific flight activity and mortality of male honey bees from two different genetic lines that are exclusively dedicated to reproduction. We show that males initiating flight at a young age experience more flight events during their lifetime. No (negative) relation between the age at flight initiation and lifespan exists, as might be predicted on the basis of the antagonistic pleiotropy theory of aging. Furthermore, we fit our data to different aging models and conclude that overall a slight deceleration of the age-dependent mortality increase at advanced ages occurs. However, mortality risk increases according to the Gompertz-Makeham model when only days with flight activity (active days) are taken into account. Our interpretation of the latter is that two mortality components act on honey bee males during flight: increasing, age-dependent deaths (possibly from wear-and-tear), and age-independent deaths (possibly due to predation). The overall mortality curve is caused by the interaction of the distribution of age at foraging initiation and the mortality function during the active (flight) lifespan.
Asunto(s)
Abejas/fisiología , Mortalidad , Envejecimiento , Animales , Abejas/genética , Vuelo Animal , Funciones de Verosimilitud , Modelos Logísticos , Longevidad/genética , Longevidad/fisiología , Masculino , Dinámica Poblacional , Reproducción , Conducta Social , Tasa de SupervivenciaRESUMEN
The initiation of foraging during the life course of honeybee workers is of central interest to understanding the division of labor in social insects, a central theme in sociobiology and behavioral research. It also provides one of the most complex phenotypic traits in biological systems because of the interaction of various external, social, and individual factors. This study reports on a comprehensive investigation of the genetic architecture of the age of foraging initiation in honeybees. It comprises an estimation of genetic variation, the study of candidate loci, and two complementary quantitative trait loci (QTL) maps using two selected, continually bred lines of honeybees. We conclude that considerable genetic variation exists between the selected lines for this central life history component. The study reveals direct pleiotropic and epistatic effects of candidate loci (including previously identified QTL for foraging behavior). Furthermore, two maps of the honeybee genome were constructed from over 400 AFLP markers. Both maps confirm the extraordinary recombinational size of the honeybee genome. On the basis of these maps, we report four new significant QTL and two more suggestive QTL that influence the initiation of foraging.