Page 331. CHAPTER FOURTEEN tu? Behavioral Genetics in Social Insects JÜRGEN GADAU GREG J. HUNT BE... more Page 331. CHAPTER FOURTEEN tu? Behavioral Genetics in Social Insects JÜRGEN GADAU GREG J. HUNT BEHAVIORAL CHANGES or pre-adaptations of individual organisms must have been a prerequisite for the evolution of sociality in insects. ...
Individual differences in learning can influence how animals respond to and communicate about the... more Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI col...
Background Parasitoid wasps have fascinating life cycles and play an important role in trophic ne... more Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. Results We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We i...
ABSTRACTCollective cognition allows animal groups to accomplish many tasks that could not be acco... more ABSTRACTCollective cognition allows animal groups to accomplish many tasks that could not be accomplished as effectively alone, such as schools of fish avoiding predators1, flocks of birds moving thousands of miles across the Earth2, and honey bee colonies collecting food from millions of flowers3. Individuals in groups utilize local information to quickly adjust to ecological changes by implicitly or explicitly communicating information with group members to form collective behavior4–6. However, individuals vary in their cognitive abilities, which influences the information each individual pays attention to or shares, thus influencing collective responses7–9. Here, we show that individual differences in learning scales to shape collective foraging behavior in honey bees by utilizing a naturally variable and heritable learning behavior called latent inhibition (LI)10. We artificially selected two distinct phenotypes: high LI bees that are better at ignoring previously unrewarding fa...
Animals must effectively balance the time they spend exploring the environment for new resources ... more Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.
The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct h... more The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct hosts are practically unknown. The wasp Aphidius ervi, a generalist koinobiont parasitoid of aphids, was introduced from Europe into Chile in the late 1970s to control agriculturally important aphid species. A recent study showed significant differences in host preference and host acceptance (infectivity) depending on the host A. ervi were reared on. In contrast, no genetic differentiation between A. ervi populations parasitizing different aphid species and aphids of the same species reared on different host plants was found in Chile. Additionally, the same study did not find any fitness effects in A. ervi if offspring were reared on a different host as their mothers. Here, we determined the effect of aphid host species (Sitobion avenae versus Acyrthosiphon pisum reared on two different host plants alfalfa and pea) on the transcriptome of adult A. ervi females. We found a large number of ...
Are we in the midst of a paradigm change in biology and have animals and plants lost their indivi... more Are we in the midst of a paradigm change in biology and have animals and plants lost their individuality, i.e., are even so-called 'typical' organisms no longer organisms in their own right? Is the study of the holobiont-host plus its symbiotic microorganisms-no longer optional, but rather an obligatory path that must be taken for a comprehensive understanding of the ecology and evolution of the individual components that make up a holobiont? Or are associated microbes merely a component of their host's environment, and the holobiont concept is just a beautiful idea that does not add much or anything to our understanding of evolution? This article explores different aspects of the concept of the holobiont. We focus on the aspect of functional integration, a central holobiont property, which is only rarely considered thoroughly. We conclude that the holobiont comes in degrees, i.e., we regard the property of being a holobiont as a continuous trait that we term holobiontness, and that holobiontness is differentiated in several dimensions. Although the holobiont represents yet another level of selection (different from classical individual or group selection because it acts on a system that is composed of multiple species), it depends on the grade of functional integration whether or not the holobiont concept helps to cast light on the various degrees of interactions between symbiotic partners.
A key requirement for social cooperation is the mitigation and/or social regulation of aggression... more A key requirement for social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behavior and head gene expression profiles. A proportion of queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to perform aggressive acts, and conflict escalated more frequently in pairs of haplometrotic queens. Whole-head RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate dif...
We present a phylogeographic study of at least six reproductively isolated lineages of new world ... more We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because their GCD requires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. This GCD system maintains genetic isolation among these interdependent lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these four GCD lineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies' ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of the GCD lineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of the GCD system. Our analyses also reveal a complex pattern of vicariance and dispersal in Pogonomyrmex harvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.
Annals of the Entomological Society of America, 1999
... Chenault) (CASC); Joshua Tree NM, L. Covington Flat (M. Knox & E. Sleeper... more ... Chenault) (CASC); Joshua Tree NM, L. Covington Flat (M. Knox & E. Sleeper) (CASC); Joshua Tree NM, U. Covington Flat (EL ... Barbara County: Santa Barbara (GE Woodhams) (CDAE); Solano County: Cold Canyon, 19 km NNW Vacaville, 120 m (SG Brady) (UCDC); Cold ...
Desaturase genes are essential for biological processes, including lipid metabolism, cell signali... more Desaturase genes are essential for biological processes, including lipid metabolism, cell signaling, and membrane fluidity regulation. Insect desaturases are particularly interesting for their role in chemical communication, and potential contribution to speciation, symbioses, and sociality. Here, we describe the acyl-CoA desaturase gene families of 15 insects, with a focus on social Hymenoptera. Phylogenetic reconstruction revealed that the insect desaturases represent an ancient gene family characterized by eight subfamilies that differ strongly in their degree of conservation and frequency of gene gain and loss. Analyses of genomic organization showed that five of these subfamilies are represented in a highly microsyntenic region conserved across holometabolous insect taxa, indicating an ancestral expansion during early insect evolution. In three subfamilies, ants exhibit particularly large expansions of genes. Despite these expansions, however, selection analyses showed that desaturase genes in all insect lineages are predominantly undergoing strong purifying selection. Finally, for three expanded subfamilies, we show that ants exhibit variation in gene expression between species, and more importantly, between sexes and castes within species. This suggests functional differentiation of these genes and a role in the regulation of reproductive division of labor in ants. The dynamic pattern of gene gain and loss of acyl-CoA desaturases in ants may reflect changes in response to ecological diversification and an increased demand for chemical signal variability. This may provide an example of how gene family expansions can contribute to lineage-specific adaptations through structural and regulatory changes acting in concert to produce new adaptive phenotypes.
Six polymorphic microsatellite loci were isolated and characterized from the temporary social par... more Six polymorphic microsatellite loci were isolated and characterized from the temporary social parasitic ant Lasius fuliginosus by a highly efficient enrichment procedure. Observed allele numbers ranged from three to 20 per locus, whereby four out of the six tested loci had more than 10 alleles and showed both observed and expected heterozygosities greater than 70%. For each locus we present suitable primer sequences. With these microsatellite markers we will be able to reveal colony and population structure of L. fuliginosus .
This article describes QTL analyses for solitary (Nasonia, a parasitoid wasp) and social hymenopt... more This article describes QTL analyses for solitary (Nasonia, a parasitoid wasp) and social hymenopteran species (honeybee and bumblebee). These exemplar QTL analyses determined the genetic basis of morphological, behavioral, and colony level traits. Mapping populations were derived either from lab crosses between highly inbred strains (Nasonia spp.), lab crosses of individuals caught in the field (bumblebees), or offspring from artificially inseminated queens from a managed honeybee population. Using these examples, we demonstrate the importance of a clear understanding of the life history, breeding, and reproductive system of the organism used for a QTL analysis, e.g., haplo-diploidy or reproductive division of labor in social insects. We lead the reader step by step through the process of multiple QTL analyses and describe potential problems and roadblocks (e.g., data handling, statistical, and biological problems) that can obscure or severely impair the results of a QTL study and how to detect and deal with those problems.In particular, we provide a way to empirically estimate the Beavis effect for a larger QTL mapping population and how to estimate a more accurate value of the explained phenotypic variance of each detected QTL using a resampling procedure.
... Biological Systems J ¨urgen Gadau and Manfred D. Laubichler School of Life Sciences, Center f... more ... Biological Systems J ¨urgen Gadau and Manfred D. Laubichler School of Life Sciences, Center for Social Dynamics and Complexity Arizona State University Tempe, AZ, USA [email protected][email protected] Why Relatedness? ...
Page 331. CHAPTER FOURTEEN tu? Behavioral Genetics in Social Insects JÜRGEN GADAU GREG J. HUNT BE... more Page 331. CHAPTER FOURTEEN tu? Behavioral Genetics in Social Insects JÜRGEN GADAU GREG J. HUNT BEHAVIORAL CHANGES or pre-adaptations of individual organisms must have been a prerequisite for the evolution of sociality in insects. ...
Individual differences in learning can influence how animals respond to and communicate about the... more Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI col...
Background Parasitoid wasps have fascinating life cycles and play an important role in trophic ne... more Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. Results We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We i...
ABSTRACTCollective cognition allows animal groups to accomplish many tasks that could not be acco... more ABSTRACTCollective cognition allows animal groups to accomplish many tasks that could not be accomplished as effectively alone, such as schools of fish avoiding predators1, flocks of birds moving thousands of miles across the Earth2, and honey bee colonies collecting food from millions of flowers3. Individuals in groups utilize local information to quickly adjust to ecological changes by implicitly or explicitly communicating information with group members to form collective behavior4–6. However, individuals vary in their cognitive abilities, which influences the information each individual pays attention to or shares, thus influencing collective responses7–9. Here, we show that individual differences in learning scales to shape collective foraging behavior in honey bees by utilizing a naturally variable and heritable learning behavior called latent inhibition (LI)10. We artificially selected two distinct phenotypes: high LI bees that are better at ignoring previously unrewarding fa...
Animals must effectively balance the time they spend exploring the environment for new resources ... more Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.
The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct h... more The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct hosts are practically unknown. The wasp Aphidius ervi, a generalist koinobiont parasitoid of aphids, was introduced from Europe into Chile in the late 1970s to control agriculturally important aphid species. A recent study showed significant differences in host preference and host acceptance (infectivity) depending on the host A. ervi were reared on. In contrast, no genetic differentiation between A. ervi populations parasitizing different aphid species and aphids of the same species reared on different host plants was found in Chile. Additionally, the same study did not find any fitness effects in A. ervi if offspring were reared on a different host as their mothers. Here, we determined the effect of aphid host species (Sitobion avenae versus Acyrthosiphon pisum reared on two different host plants alfalfa and pea) on the transcriptome of adult A. ervi females. We found a large number of ...
Are we in the midst of a paradigm change in biology and have animals and plants lost their indivi... more Are we in the midst of a paradigm change in biology and have animals and plants lost their individuality, i.e., are even so-called 'typical' organisms no longer organisms in their own right? Is the study of the holobiont-host plus its symbiotic microorganisms-no longer optional, but rather an obligatory path that must be taken for a comprehensive understanding of the ecology and evolution of the individual components that make up a holobiont? Or are associated microbes merely a component of their host's environment, and the holobiont concept is just a beautiful idea that does not add much or anything to our understanding of evolution? This article explores different aspects of the concept of the holobiont. We focus on the aspect of functional integration, a central holobiont property, which is only rarely considered thoroughly. We conclude that the holobiont comes in degrees, i.e., we regard the property of being a holobiont as a continuous trait that we term holobiontness, and that holobiontness is differentiated in several dimensions. Although the holobiont represents yet another level of selection (different from classical individual or group selection because it acts on a system that is composed of multiple species), it depends on the grade of functional integration whether or not the holobiont concept helps to cast light on the various degrees of interactions between symbiotic partners.
A key requirement for social cooperation is the mitigation and/or social regulation of aggression... more A key requirement for social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behavior and head gene expression profiles. A proportion of queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to perform aggressive acts, and conflict escalated more frequently in pairs of haplometrotic queens. Whole-head RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate dif...
We present a phylogeographic study of at least six reproductively isolated lineages of new world ... more We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because their GCD requires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. This GCD system maintains genetic isolation among these interdependent lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these four GCD lineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies' ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of the GCD lineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of the GCD system. Our analyses also reveal a complex pattern of vicariance and dispersal in Pogonomyrmex harvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.
Annals of the Entomological Society of America, 1999
... Chenault) (CASC); Joshua Tree NM, L. Covington Flat (M. Knox & E. Sleeper... more ... Chenault) (CASC); Joshua Tree NM, L. Covington Flat (M. Knox & E. Sleeper) (CASC); Joshua Tree NM, U. Covington Flat (EL ... Barbara County: Santa Barbara (GE Woodhams) (CDAE); Solano County: Cold Canyon, 19 km NNW Vacaville, 120 m (SG Brady) (UCDC); Cold ...
Desaturase genes are essential for biological processes, including lipid metabolism, cell signali... more Desaturase genes are essential for biological processes, including lipid metabolism, cell signaling, and membrane fluidity regulation. Insect desaturases are particularly interesting for their role in chemical communication, and potential contribution to speciation, symbioses, and sociality. Here, we describe the acyl-CoA desaturase gene families of 15 insects, with a focus on social Hymenoptera. Phylogenetic reconstruction revealed that the insect desaturases represent an ancient gene family characterized by eight subfamilies that differ strongly in their degree of conservation and frequency of gene gain and loss. Analyses of genomic organization showed that five of these subfamilies are represented in a highly microsyntenic region conserved across holometabolous insect taxa, indicating an ancestral expansion during early insect evolution. In three subfamilies, ants exhibit particularly large expansions of genes. Despite these expansions, however, selection analyses showed that desaturase genes in all insect lineages are predominantly undergoing strong purifying selection. Finally, for three expanded subfamilies, we show that ants exhibit variation in gene expression between species, and more importantly, between sexes and castes within species. This suggests functional differentiation of these genes and a role in the regulation of reproductive division of labor in ants. The dynamic pattern of gene gain and loss of acyl-CoA desaturases in ants may reflect changes in response to ecological diversification and an increased demand for chemical signal variability. This may provide an example of how gene family expansions can contribute to lineage-specific adaptations through structural and regulatory changes acting in concert to produce new adaptive phenotypes.
Six polymorphic microsatellite loci were isolated and characterized from the temporary social par... more Six polymorphic microsatellite loci were isolated and characterized from the temporary social parasitic ant Lasius fuliginosus by a highly efficient enrichment procedure. Observed allele numbers ranged from three to 20 per locus, whereby four out of the six tested loci had more than 10 alleles and showed both observed and expected heterozygosities greater than 70%. For each locus we present suitable primer sequences. With these microsatellite markers we will be able to reveal colony and population structure of L. fuliginosus .
This article describes QTL analyses for solitary (Nasonia, a parasitoid wasp) and social hymenopt... more This article describes QTL analyses for solitary (Nasonia, a parasitoid wasp) and social hymenopteran species (honeybee and bumblebee). These exemplar QTL analyses determined the genetic basis of morphological, behavioral, and colony level traits. Mapping populations were derived either from lab crosses between highly inbred strains (Nasonia spp.), lab crosses of individuals caught in the field (bumblebees), or offspring from artificially inseminated queens from a managed honeybee population. Using these examples, we demonstrate the importance of a clear understanding of the life history, breeding, and reproductive system of the organism used for a QTL analysis, e.g., haplo-diploidy or reproductive division of labor in social insects. We lead the reader step by step through the process of multiple QTL analyses and describe potential problems and roadblocks (e.g., data handling, statistical, and biological problems) that can obscure or severely impair the results of a QTL study and how to detect and deal with those problems.In particular, we provide a way to empirically estimate the Beavis effect for a larger QTL mapping population and how to estimate a more accurate value of the explained phenotypic variance of each detected QTL using a resampling procedure.
... Biological Systems J ¨urgen Gadau and Manfred D. Laubichler School of Life Sciences, Center f... more ... Biological Systems J ¨urgen Gadau and Manfred D. Laubichler School of Life Sciences, Center for Social Dynamics and Complexity Arizona State University Tempe, AZ, USA [email protected][email protected] Why Relatedness? ...
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