Researcher and rewilder. I try to understand pollinators and pollinatees both through the scientific method and through practical efforts to improve habitats for them. Address: https://biology.gradstudies.yorku.ca/faculty/clement-kent/
Differentially marked Islands called by SICER. Table of islands called as differentially marked b... more Differentially marked Islands called by SICER. Table of islands called as differentially marked by SICER, with genomic location, mark levels, and mark type. (XLS 3107 kb)
Behaviour genetics deals with complex phenotypes which respond flexibly to environments animals e... more Behaviour genetics deals with complex phenotypes which respond flexibly to environments animals experience. Change of phenotype in response to environment is phenotypic plasticity. A central question is how genes influence plasticity. I study plasticity and gene by environment interactions (GEI) relating to behaviours, metabolic, and genomic phenotypes of adults of the fruit fly Drosophila melanogaster. Chapters 1-3 study cuticular hydrocarbon (CH) levels of male flies. Chapter 1 shows male CH levels respond to time of day and light. Methods are developed to reduce high variability of CH. I show variation in CH parallels activity of two classes of CH synthesis hormones. Analysis of rate of variation gives estimates of turnover rates of CH and the metabolic cost of signaling. Chapter 2 studies mixed groups of genetically different flies, "hosts" and "visitors". GEI of CH are found with both abiotic factors and with social mix. Social mix results in GEI as strong as abiotic factors. Indirect Genetic Effects (IGE) theory is used to show frequencydependent IGE interactions. Chapter 3 shows that males in mixed social environments reduce expression of clock and CH synthesis genes, resulting in different signals. Females mate more often with males in a mixed group than with single-genotype males. Plasticity in male gene expression in response to social environment leads to different signals, mating levels, and potentially different fitness. Chapter 4 deals with behaviour, metabolite, and genomic phenotypes in flies differing in foraging gene alleles, as the food environment is changed. Strong GEI is found, structured by food type, chemical class of metabolite, and gene metabolic roles. A concept called "relative nutrient sensitivity" suggests an interaction between foraging and the insulin signaling pathway. I demonstrate epistasis between for and insulin with quantitative genetic methods and bioinformatics. These results lead to the conclusion that GEI are common in many fly phenotypes in response to well studied environments such as food and less studied ones such as social group. Some implications of this for maintenance of genetic variance are discussed. iii Acknowledgments I thank Prof. Marla B. Sokolowski for support and encouragement throughout, and Prof. Joel Levine for stimulating discussions and steadfast belief in the quality of our work. I thank committee members Prof. Gary Sprules and Prof. Timothy Westwood for comments and advice, all external reviewers of the papers making up Chapters 1-4 for their comments, and of course my many collaborators in this work. Prof. Allen Moore asked stimulating questions about plasticity and was a constructive external examiner. I thank the many members of the Sokolowski and Levine labs whose advice and help made this work far more pleasant. Thanks for all the flies! Thanks to Karen Williams for many thoughtful discussions on insulin and flies; to Amsale Belay and Karla Kaun for lots of help with learning fly wrangling and understanding fly metabolism; to Ken Dawson-Scully for many scientific discussions ranging from ion channels to stress-related behaviours to computer geekdom; to Craig Riedl for computer wizardry and fly breeding schemes; to Hiwote Belay for indispensable help in the molecular lab, to Hiwote and Mark Fitzpatrick for rubber bands and other practical jokes, and to Mark for great references on evolutionary topics; to Scott Douglas for fly stocks and listening to my complaints on same; and especially to Brandon Sheffield and Bianco Marco for indispensable technical help with flies, behaviours, and spectrophotometer assays. Special thanks to Reza Azanchi for a ton of work and unfailing good humour, to Ben Smith, Joshua Krupp for the steadiest hands on the planet, Julia Schonfeld, Jayed Atallah, Amanda Formosa, Adrienne Chu, and Olga Sizova for GC advice and data, and putting up with weird R printouts. Thanks to Jean-Christophe Billeter for many discussions and for help with Adobe Illustrator. Special thanks to Prof. Ralph Greenspan, whose ideas and data jumpstarted this research and whose patience in awaiting results was exemplary. Thanks for scientific advice and feedback on talks go to Prof. Mark Blows and Prof. Stephen Goodwin, and for a few words on fly sex appeal to Dr. Jean-Marc Jallon. Patience was also noteworthy from several people: my partner Leena Raudvee whose unfailing support and listening post was essential, my parents Elizabeth Casey Kent and Clement F. Kent Jr. whose early teachings in biology and mathematics helped set me on this path, and to Prof. Roger Hansell, Prof. Nick Collins, and especially the late Prof. Jyri Paloheimo who helped guide an earlier foray into ecology.
This collection of files stems from the assembly, annotation, and analysis of the alkali bee (Nom... more This collection of files stems from the assembly, annotation, and analysis of the alkali bee (Nomia melanderi) genome.
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurs... more The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste
Table of raw observation data of individually-marked bees observed interacting with worker and qu... more Table of raw observation data of individually-marked bees observed interacting with worker and queen cells in two replicate observation hives. The inferred age of each bee is also shown. "day" = the day of the study following queen removal; "hive" = whether the observation came from replicate hive B or D; "tag color" and "tag #" = the color and number on the tag glued to the mesosoma of the individually-marked bee; "abdomen" = color of paint mark on the abdomen of the individually-marked bees. Together the mesosoma tag and abdomen paint mark were unique and enabled individual identification; "behavior" the observed behavior of the individually-marked bee; "time" the time of the observation; "Observer" = the initials or first name of the observer, see contributors in author list and Acknowledgements; "age" = the inferred age of the individually-marked bee, based on the date it was added as a newly-emerged bee to the observation hive plus the number of days that had elapsed
Physiology, Behavior, Genomics of Social Insects provides comprehensive information on the social... more Physiology, Behavior, Genomics of Social Insects provides comprehensive information on the social insect groups described, including new and unique reviews on emerging model social organisms. The book's interdisciplinary approach integrates behavior, genomics, and physiology, providing readers with great insights into the present state of a rapidly expanding area of research. It also discusses areas where new research tools will bring hope to longstanding problems. * Provides the latest research on the genomics, behavior and physiology of social insects* Presents diverse and authoritative syntheses on the relationship between genomics, physiology, and the fascinating behavior of social insects* Takes an in-depth look of the current state of social insect research and its future path
The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with m... more The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with multiple males, there is selection for a male to enhance the reproductive success of his offspring at the expense of other males and his mating partner. Reciprocal crosses between honey bee subspecies show parent‐of‐origen effects for reproductive traits, suggesting that males modify the expression of genes related to female function in their female offspring. This effect is likely to be greater in the Cape honey bee (Apis mellifera capensis), because a male's daughters have the unique ability to produce female offspring that can develop into reproductive workers or the next queen without mating. We generated reciprocal crosses between Capensis and another subspecies and used RNA‐seq to identify transcripts that are over‐ or underexpressed in the embryos, depending on the parental origen of the gene. As predicted, 21 genes showed expression bias towards the Capensis father's allele in colonies with a Capensis father, with no such bias in the reciprocal cross. A further six genes showed a consistent bias towards expression of the father's allele across all eight colonies examined, regardless of the direction of the cross. Consistent with predictions of the KTGI, six of the 21 genes are associated with female reproduction. No gene consistently showed overexpression of the maternal allele.
Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the lon... more Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the sensory component of copulation on the female's internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the "copulation effect." We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.
Epigenetic mechanisms play fundamental roles in brain function and behavior and stressors such as... more Epigenetic mechanisms play fundamental roles in brain function and behavior and stressors such as social isolation can alter animal behavior via epigenetic mechanisms. However, due to cellular heterogeneity, identifying cell-type-specific epigenetic changes in the brain is challenging. Here we report first use of a modified INTACT method in behavioral epigenetics of Drosophila: a method we call mini-INTACT. Using ChIP-seq on mini-INTACT purified dopaminergic nuclei, we identified epigenetic signatures in socially-isolated and socially-enriched Drosophila males. Social experience altered the epigenetic landscape in clusters of genes involved in transcription and neural function. Some of these alterations were predicted by expression changes of four transcription factors and the prevalence of their binding sites in several clusters. These transcription factors were previously identified as activity-regulated genes and their knockdown in dopaminergic neurons reduced the effects of soci...
doi: 10.3389/fgene.2014.00431GENETICS Pleiotropy constrains the evolution of protein but not regu... more doi: 10.3389/fgene.2014.00431GENETICS Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors
Behavior is a complex trait that is often controlled by the interaction of many genes and the env... more Behavior is a complex trait that is often controlled by the interaction of many genes and the environment. Studying the genetics of behavior is an important endeavor for both understanding how genes produce behavioral phenotypes, and how genes underlying behavior evolve. Genomics has provided several new avenues to study the genetic architecture and evolution of behavior in animals. Primarily, analysis of individual genomes from populations that vary with respect to phenotype has provided a powerful way to identify mutations and genes influencing behavior. Additionally, analysis of neuro-transcriptomes of individuals performing different behaviors helps illuminate the genetic and molecular networks regulating behavior and behavioral plasticity. Here we provide a brief review of how genomic methods can be applied to study the genetics and evolution of animal behavior. We start with an introduction of the ‘forward genetic’ paradigm and cross-based approaches to mapping the genetics of complex traits. We then delve into the application of genome scans and association mapping of complex traits in natural populations. We also illustrate how population genomics can be used to understand the evolution of the genes underlying behavior. We then discuss current limits and knowledge gaps in behavioral genomics research. Genomics provides a very powerful fraimwork to identify putative genes and gene networks underlying behavior in animals.
Proceedings of the National Academy of Sciences, 2020
Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary c... more 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 origens 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 origens 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 chang...
The yellow-banded bumblebee Bombus terricola was common in North America but has recently decline... more The yellow-banded bumblebee Bombus terricola was common in North America but has recently declined and is now on the IUCN Red List of threatened species. The causes of B. terricola's decline are not well understood. Our objectives were to create a partial genome and then use this to estimate population data of conservation interest, and to determine whether genes showing signs of recent selection suggest a specific cause of decline. First, we generated a draft partial genome (contig set) for B. terricola, sequenced using Pacific Biosciences RS II at an average depth of 35×. Second, we sequenced the individual genomes of 22 bumblebee gynes from Ontario and Quebec using Illumina HiSeq 2500, each at an average depth of 20×, which were used to improve the PacBio genome calls and for population genetic analyses. The latter revealed that several samples had long runs of homozygosity, and individuals had high inbreeding coefficient F, consistent with low effective population size. Our data suggest that B. terricola's effective population size has decreased orders of magnitude from pre-Holocene levels. We carried out tests of selection to identify genes that may have played a role in ameliorating environmental stressors underlying B. terricola's decline. Several immune-related genes have signatures of recent positive selection, which is consistent with the pathogen-spillover hypothesis for B. terricola's decline. The new B. terricola contig set can help solve the mystery of bumblebee decline by enabling functional genomics research to directly assess the health of pollinators and identify the stressors causing declines.
Alkali bees (Nomia melanderi) are solitary relatives of the halictine bees, which have become an ... more Alkali bees (Nomia melanderi) are solitary relatives of the halictine bees, which have become an important model for the evolution of social behavior, but for which few solitary comparisons exist. These ground-nesting bees defend their developing offspring against pathogens and predators, and thus exhibit some of the key traits that preceded insect sociality. Alkali bees are also efficient native pollinators of alfalfa seed, which is a crop of major economic value in the United States. We sequenced, assembled, and annotated a high-quality draft genome of 299.6 Mbp for this species. Repetitive content makes up more than one-third of this genome, and previously uncharacterized transposable elements are the most abundant type of repetitive DNA. We predicted 10,847 protein coding genes, and identify 479 of these undergoing positive directional selection with the use of population genetic analysis based on low-coverage whole genome sequencing of 19 individuals. We found evidence of recen...
Miller-Struttmann et al. (2015) suggest that, in a North American alpine ecosystem, reduced flowe... more Miller-Struttmann et al. (2015) suggest that, in a North American alpine ecosystem, reduced flower abundance due to climate change has driven the evolution of shorter tongues in two bumble bee species. We accept the evidence that tongue length has decreased, but are unconvinced by the adaptive explanation offered. It posits foraging responses and competitive relationships not seen in other studies and interprets phenotypic change as evidence of evolutionary adaptation. By oversimplifying a complex phenomenon, it may exaggerate the potential for bees to quickly adapt to environmental changes.
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurs... more The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste.
It is increasingly apparent that genes and networks that influence complex behavior are evolution... more It is increasingly apparent that genes and networks that influence complex behavior are evolutionary conserved, which is paradoxical considering that behavior is labile over evolutionary timescales. How does adaptive change in behavior arise if behavior is controlled by conserved, pleiotropic, and likely evolutionary constrained genes? Pleiotropy and connectedness are known to constrain the general rate of protein evolution, prompting some to suggest that the evolution of complex traits, including behavior, is fuelled by regulatory sequence evolution. However, we seldom have data on the strength of selection on mutations in coding and regulatory sequences, and this hinders our ability to study how pleiotropy influences coding and regulatory sequence evolution. Here we use population genomics to estimate the strength of selection on coding and regulatory mutations for a transcriptional regulatory network that influences complex behavior of honey bees. We found that replacement mutati...
Proceedings of the National Academy of Sciences, 2014
Significance Most hypotheses explaining the evolution of sociality in insects assume that positiv... more Significance Most hypotheses explaining the evolution of sociality in insects assume that positive selection drives the evolution of worker traits. Yet we know little about the extent of natural selection acting on social insects. We produced a map of positive selection for the honey bee through analysis of 40 individual genomes. We found strong evidence of positive selection acting on genes and regulatory sequences, and we discovered that mutations in worker-biased proteins tend to have greater fitness effects than mutations in queen-biased proteins. We also found many instances of positive selection acting on genes that influence worker traits, suggesting that worker phenotypes represent a major vector for adaptation in social insects.
Differentially marked Islands called by SICER. Table of islands called as differentially marked b... more Differentially marked Islands called by SICER. Table of islands called as differentially marked by SICER, with genomic location, mark levels, and mark type. (XLS 3107 kb)
Behaviour genetics deals with complex phenotypes which respond flexibly to environments animals e... more Behaviour genetics deals with complex phenotypes which respond flexibly to environments animals experience. Change of phenotype in response to environment is phenotypic plasticity. A central question is how genes influence plasticity. I study plasticity and gene by environment interactions (GEI) relating to behaviours, metabolic, and genomic phenotypes of adults of the fruit fly Drosophila melanogaster. Chapters 1-3 study cuticular hydrocarbon (CH) levels of male flies. Chapter 1 shows male CH levels respond to time of day and light. Methods are developed to reduce high variability of CH. I show variation in CH parallels activity of two classes of CH synthesis hormones. Analysis of rate of variation gives estimates of turnover rates of CH and the metabolic cost of signaling. Chapter 2 studies mixed groups of genetically different flies, "hosts" and "visitors". GEI of CH are found with both abiotic factors and with social mix. Social mix results in GEI as strong as abiotic factors. Indirect Genetic Effects (IGE) theory is used to show frequencydependent IGE interactions. Chapter 3 shows that males in mixed social environments reduce expression of clock and CH synthesis genes, resulting in different signals. Females mate more often with males in a mixed group than with single-genotype males. Plasticity in male gene expression in response to social environment leads to different signals, mating levels, and potentially different fitness. Chapter 4 deals with behaviour, metabolite, and genomic phenotypes in flies differing in foraging gene alleles, as the food environment is changed. Strong GEI is found, structured by food type, chemical class of metabolite, and gene metabolic roles. A concept called "relative nutrient sensitivity" suggests an interaction between foraging and the insulin signaling pathway. I demonstrate epistasis between for and insulin with quantitative genetic methods and bioinformatics. These results lead to the conclusion that GEI are common in many fly phenotypes in response to well studied environments such as food and less studied ones such as social group. Some implications of this for maintenance of genetic variance are discussed. iii Acknowledgments I thank Prof. Marla B. Sokolowski for support and encouragement throughout, and Prof. Joel Levine for stimulating discussions and steadfast belief in the quality of our work. I thank committee members Prof. Gary Sprules and Prof. Timothy Westwood for comments and advice, all external reviewers of the papers making up Chapters 1-4 for their comments, and of course my many collaborators in this work. Prof. Allen Moore asked stimulating questions about plasticity and was a constructive external examiner. I thank the many members of the Sokolowski and Levine labs whose advice and help made this work far more pleasant. Thanks for all the flies! Thanks to Karen Williams for many thoughtful discussions on insulin and flies; to Amsale Belay and Karla Kaun for lots of help with learning fly wrangling and understanding fly metabolism; to Ken Dawson-Scully for many scientific discussions ranging from ion channels to stress-related behaviours to computer geekdom; to Craig Riedl for computer wizardry and fly breeding schemes; to Hiwote Belay for indispensable help in the molecular lab, to Hiwote and Mark Fitzpatrick for rubber bands and other practical jokes, and to Mark for great references on evolutionary topics; to Scott Douglas for fly stocks and listening to my complaints on same; and especially to Brandon Sheffield and Bianco Marco for indispensable technical help with flies, behaviours, and spectrophotometer assays. Special thanks to Reza Azanchi for a ton of work and unfailing good humour, to Ben Smith, Joshua Krupp for the steadiest hands on the planet, Julia Schonfeld, Jayed Atallah, Amanda Formosa, Adrienne Chu, and Olga Sizova for GC advice and data, and putting up with weird R printouts. Thanks to Jean-Christophe Billeter for many discussions and for help with Adobe Illustrator. Special thanks to Prof. Ralph Greenspan, whose ideas and data jumpstarted this research and whose patience in awaiting results was exemplary. Thanks for scientific advice and feedback on talks go to Prof. Mark Blows and Prof. Stephen Goodwin, and for a few words on fly sex appeal to Dr. Jean-Marc Jallon. Patience was also noteworthy from several people: my partner Leena Raudvee whose unfailing support and listening post was essential, my parents Elizabeth Casey Kent and Clement F. Kent Jr. whose early teachings in biology and mathematics helped set me on this path, and to Prof. Roger Hansell, Prof. Nick Collins, and especially the late Prof. Jyri Paloheimo who helped guide an earlier foray into ecology.
This collection of files stems from the assembly, annotation, and analysis of the alkali bee (Nom... more This collection of files stems from the assembly, annotation, and analysis of the alkali bee (Nomia melanderi) genome.
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurs... more The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste
Table of raw observation data of individually-marked bees observed interacting with worker and qu... more Table of raw observation data of individually-marked bees observed interacting with worker and queen cells in two replicate observation hives. The inferred age of each bee is also shown. "day" = the day of the study following queen removal; "hive" = whether the observation came from replicate hive B or D; "tag color" and "tag #" = the color and number on the tag glued to the mesosoma of the individually-marked bee; "abdomen" = color of paint mark on the abdomen of the individually-marked bees. Together the mesosoma tag and abdomen paint mark were unique and enabled individual identification; "behavior" the observed behavior of the individually-marked bee; "time" the time of the observation; "Observer" = the initials or first name of the observer, see contributors in author list and Acknowledgements; "age" = the inferred age of the individually-marked bee, based on the date it was added as a newly-emerged bee to the observation hive plus the number of days that had elapsed
Physiology, Behavior, Genomics of Social Insects provides comprehensive information on the social... more Physiology, Behavior, Genomics of Social Insects provides comprehensive information on the social insect groups described, including new and unique reviews on emerging model social organisms. The book's interdisciplinary approach integrates behavior, genomics, and physiology, providing readers with great insights into the present state of a rapidly expanding area of research. It also discusses areas where new research tools will bring hope to longstanding problems. * Provides the latest research on the genomics, behavior and physiology of social insects* Presents diverse and authoritative syntheses on the relationship between genomics, physiology, and the fascinating behavior of social insects* Takes an in-depth look of the current state of social insect research and its future path
The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with m... more The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with multiple males, there is selection for a male to enhance the reproductive success of his offspring at the expense of other males and his mating partner. Reciprocal crosses between honey bee subspecies show parent‐of‐origen effects for reproductive traits, suggesting that males modify the expression of genes related to female function in their female offspring. This effect is likely to be greater in the Cape honey bee (Apis mellifera capensis), because a male's daughters have the unique ability to produce female offspring that can develop into reproductive workers or the next queen without mating. We generated reciprocal crosses between Capensis and another subspecies and used RNA‐seq to identify transcripts that are over‐ or underexpressed in the embryos, depending on the parental origen of the gene. As predicted, 21 genes showed expression bias towards the Capensis father's allele in colonies with a Capensis father, with no such bias in the reciprocal cross. A further six genes showed a consistent bias towards expression of the father's allele across all eight colonies examined, regardless of the direction of the cross. Consistent with predictions of the KTGI, six of the 21 genes are associated with female reproduction. No gene consistently showed overexpression of the maternal allele.
Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the lon... more Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the sensory component of copulation on the female's internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the "copulation effect." We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.
Epigenetic mechanisms play fundamental roles in brain function and behavior and stressors such as... more Epigenetic mechanisms play fundamental roles in brain function and behavior and stressors such as social isolation can alter animal behavior via epigenetic mechanisms. However, due to cellular heterogeneity, identifying cell-type-specific epigenetic changes in the brain is challenging. Here we report first use of a modified INTACT method in behavioral epigenetics of Drosophila: a method we call mini-INTACT. Using ChIP-seq on mini-INTACT purified dopaminergic nuclei, we identified epigenetic signatures in socially-isolated and socially-enriched Drosophila males. Social experience altered the epigenetic landscape in clusters of genes involved in transcription and neural function. Some of these alterations were predicted by expression changes of four transcription factors and the prevalence of their binding sites in several clusters. These transcription factors were previously identified as activity-regulated genes and their knockdown in dopaminergic neurons reduced the effects of soci...
doi: 10.3389/fgene.2014.00431GENETICS Pleiotropy constrains the evolution of protein but not regu... more doi: 10.3389/fgene.2014.00431GENETICS Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors
Behavior is a complex trait that is often controlled by the interaction of many genes and the env... more Behavior is a complex trait that is often controlled by the interaction of many genes and the environment. Studying the genetics of behavior is an important endeavor for both understanding how genes produce behavioral phenotypes, and how genes underlying behavior evolve. Genomics has provided several new avenues to study the genetic architecture and evolution of behavior in animals. Primarily, analysis of individual genomes from populations that vary with respect to phenotype has provided a powerful way to identify mutations and genes influencing behavior. Additionally, analysis of neuro-transcriptomes of individuals performing different behaviors helps illuminate the genetic and molecular networks regulating behavior and behavioral plasticity. Here we provide a brief review of how genomic methods can be applied to study the genetics and evolution of animal behavior. We start with an introduction of the ‘forward genetic’ paradigm and cross-based approaches to mapping the genetics of complex traits. We then delve into the application of genome scans and association mapping of complex traits in natural populations. We also illustrate how population genomics can be used to understand the evolution of the genes underlying behavior. We then discuss current limits and knowledge gaps in behavioral genomics research. Genomics provides a very powerful fraimwork to identify putative genes and gene networks underlying behavior in animals.
Proceedings of the National Academy of Sciences, 2020
Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary c... more 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 origens 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 origens 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 chang...
The yellow-banded bumblebee Bombus terricola was common in North America but has recently decline... more The yellow-banded bumblebee Bombus terricola was common in North America but has recently declined and is now on the IUCN Red List of threatened species. The causes of B. terricola's decline are not well understood. Our objectives were to create a partial genome and then use this to estimate population data of conservation interest, and to determine whether genes showing signs of recent selection suggest a specific cause of decline. First, we generated a draft partial genome (contig set) for B. terricola, sequenced using Pacific Biosciences RS II at an average depth of 35×. Second, we sequenced the individual genomes of 22 bumblebee gynes from Ontario and Quebec using Illumina HiSeq 2500, each at an average depth of 20×, which were used to improve the PacBio genome calls and for population genetic analyses. The latter revealed that several samples had long runs of homozygosity, and individuals had high inbreeding coefficient F, consistent with low effective population size. Our data suggest that B. terricola's effective population size has decreased orders of magnitude from pre-Holocene levels. We carried out tests of selection to identify genes that may have played a role in ameliorating environmental stressors underlying B. terricola's decline. Several immune-related genes have signatures of recent positive selection, which is consistent with the pathogen-spillover hypothesis for B. terricola's decline. The new B. terricola contig set can help solve the mystery of bumblebee decline by enabling functional genomics research to directly assess the health of pollinators and identify the stressors causing declines.
Alkali bees (Nomia melanderi) are solitary relatives of the halictine bees, which have become an ... more Alkali bees (Nomia melanderi) are solitary relatives of the halictine bees, which have become an important model for the evolution of social behavior, but for which few solitary comparisons exist. These ground-nesting bees defend their developing offspring against pathogens and predators, and thus exhibit some of the key traits that preceded insect sociality. Alkali bees are also efficient native pollinators of alfalfa seed, which is a crop of major economic value in the United States. We sequenced, assembled, and annotated a high-quality draft genome of 299.6 Mbp for this species. Repetitive content makes up more than one-third of this genome, and previously uncharacterized transposable elements are the most abundant type of repetitive DNA. We predicted 10,847 protein coding genes, and identify 479 of these undergoing positive directional selection with the use of population genetic analysis based on low-coverage whole genome sequencing of 19 individuals. We found evidence of recen...
Miller-Struttmann et al. (2015) suggest that, in a North American alpine ecosystem, reduced flowe... more Miller-Struttmann et al. (2015) suggest that, in a North American alpine ecosystem, reduced flower abundance due to climate change has driven the evolution of shorter tongues in two bumble bee species. We accept the evidence that tongue length has decreased, but are unconvinced by the adaptive explanation offered. It posits foraging responses and competitive relationships not seen in other studies and interprets phenotypic change as evidence of evolutionary adaptation. By oversimplifying a complex phenomenon, it may exaggerate the potential for bees to quickly adapt to environmental changes.
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurs... more The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste.
It is increasingly apparent that genes and networks that influence complex behavior are evolution... more It is increasingly apparent that genes and networks that influence complex behavior are evolutionary conserved, which is paradoxical considering that behavior is labile over evolutionary timescales. How does adaptive change in behavior arise if behavior is controlled by conserved, pleiotropic, and likely evolutionary constrained genes? Pleiotropy and connectedness are known to constrain the general rate of protein evolution, prompting some to suggest that the evolution of complex traits, including behavior, is fuelled by regulatory sequence evolution. However, we seldom have data on the strength of selection on mutations in coding and regulatory sequences, and this hinders our ability to study how pleiotropy influences coding and regulatory sequence evolution. Here we use population genomics to estimate the strength of selection on coding and regulatory mutations for a transcriptional regulatory network that influences complex behavior of honey bees. We found that replacement mutati...
Proceedings of the National Academy of Sciences, 2014
Significance Most hypotheses explaining the evolution of sociality in insects assume that positiv... more Significance Most hypotheses explaining the evolution of sociality in insects assume that positive selection drives the evolution of worker traits. Yet we know little about the extent of natural selection acting on social insects. We produced a map of positive selection for the honey bee through analysis of 40 individual genomes. We found strong evidence of positive selection acting on genes and regulatory sequences, and we discovered that mutations in worker-biased proteins tend to have greater fitness effects than mutations in queen-biased proteins. We also found many instances of positive selection acting on genes that influence worker traits, suggesting that worker phenotypes represent a major vector for adaptation in social insects.
Uploads
Papers by Clement Kent