SIBO: A Social Insect Behavior Ontology for Ants and Bees

Christopher D. Smith Ph.D.Assistant Professor Bioinformatics

San Francisco State University

San Francisco, CA 94132

smithcd@sfsu.edu

Drosophila Heterochromatin Genome ProjectLawrence Berkeley National LabBerkeley, CA 94720

www.dhgp.org

cdsmith@fruitfly.org

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Drosophila melanogaster• 100 years of experimental data

• ‘Complete’ sequenced genome

• Many well-characterized behavior & other phenotypes

• Microarray & other large scale datasets

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Adams & Venter et. al. Science. 2000 Mar 24;287(5461):2185-95.

Genes Often Very Conserved in Metazoans• Eyeless is a classic

example– No eyes in flies, mice

– Human Blindness (Aniridia)

• Numerous Other examples– Alcoholism

• cheapdate = cAMP signaling• LUSH = odorant receptor

– Learning & Memory• dunce = cAMP metabolism

– Limb Development (Homeotic)

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Cooperativity: D. melanogaster dunce gene involved in learning & group behavior• dunce = cAMP phosphodiesterase

• ‘Search Aggregation’ in Drosophila: group advantage in finding good Tinette & Robichon. Genes Brain Behav. 2004 Feb;3(1):39-50.

• dunce overexpressed on worker bees relative to queen in beesJudice & Pereira. Insect Molecular Biology (2006) 15 (1), 33-44.

• dunce ortholog & dunce-like genes related to schizophrenia in humans Millar & Morteous. Science Vol.310. no. 5751, pp. 1187.

Numerous Insect Genomes Available

Million Years

Eusocial Insects Are Overdue for Genomics• Extensive Natural History & Literature

• Behavior Assays Already Developed

• Extensive Epigenetic Caste Regulation– Lifespan– Morphology– Complex Social Behavior

• Leverage Drosophila and use genetic, genomic, phenotype data

• Social Insect Similarities to Humans– Dominant global species– Individualism– Slavery, Policing reviewed in “The Ants” E. O Wilson

– Agriculture Mueller & Schultz. Science, v281:2034– Teaching Franks & Richardson. Nature. v439:153

>11,500 Ant species>25,000 Bee species>2800 Termite Species

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Grimaldie & EngelEvolution of the Insects

Cambridge University Press

Eusocial Insects Differeniate into Castes with Distinct Behaviors & Shapes

Image Credit : Amy Beaton, Rubin Labhttp://www.bdgp.org/cgi-bin/ex/insitu.pl

• Eusocial Hallmarks– Division of labor- Workers, Soldier, Queens, etc…– Sterile Castes (not req’d)- Single & Multiple Queens possible– Multiple generations lives in nest - Older generations care for younger

• Social behavior NOT genetically defined– Eusocial behavior has arisen many times in different species– Genetic predisposition, but no ‘hard-corded’ castes– Castes are temporally regulated in some species

• Behavior is epigenetically regulated– Genetically identical individuals express different phenotypes

Caste Programming Depend on Hormones & Environment Cues

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Abouheif & Wray Evolution of the Gene Network Underlying Wing Polyphenism in Ants

Science 12 July 2002:Vol. 297. no. 5579, pp. 249 - 252

JH = Juvenile Hormone

Covergent Behaviors in Ants & Bees

Worker & Queen Bees Express Unique Gene Subsets

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Wheeler et. al. Expression profiles during honeybee caste determinationGenomeBiology2000, 2(1):research0001.1-0001.6

• Genetically identical animals exhibit widely varied gene expression profiles

• Numerous caste specific genes have been identified in bees, ants & termites

•With completion of ‘beenome’ many more behavioral microarray expts. planned

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Identification of Putative Orthologs TBLASTN approach using the Comparative Genomics Library (CGL) Best ‘multiple-hit’ used to determine orthologous exons Orthologous introns inferred when both flanking exons are found

CG40919

Behaviors can be linked to SNPs

• Africanized bees

– Pursue Enemy 10-30x further

– More reactive to color, movement

– 4-10x stinging

– Disengage less

– Alert quickly

– Larger defense perimeter

• Using comparative annotation we can link ‘Africanized’ SNPs to gene and regulatory annotations

– e.g. Dopamine receptor mutations • DRD4

– e.g. Serotonin promoter polymorphism• hSlc6a4,dSerT

Disengagement

Perception

Orientation

1o Discriminationor Identification

AlertRecruitment

Approach

2o Discriminationor IdentificationThreat

ATTACK!

Adapted from Breed & Hunt2004. Annu. Rev. Entolom. 49:271-98

Seeding the Ontology• Currently only 100

terms

• Estimated 3500 behaviors in ants and bees

• Derived from Drosophila GO behavior terms and bee/ant literature

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Link Behaviors to ‘Language’ Genes

• Ants have more chemical producing glands than any known organism

– Queens can chemically inhibit fertility through colony

– Queens can call ‘group alarm’ for attack & defense

– Workers can communicate novel information to others back and forth (i.e. teaching)

• Link Behaviors to Chemicals– e.g. ‘Mortician Ants’ respond

to oleate from decomposition

Reviewed in Holldobler & Wilson, The Ants, 1990

Eusocial Insects Use a Complex Chemical Language that is Genetically Defined

• Language is an important aspect of social evolution across taxa– High-density– Peer Conflict Resolution– Division of labor– Group Defense

• Ants Can ‘Read’ Hundreds of Chemicals– Few receptors known

• Biogenic Amines– e.g. octapamine involved in

honeybee aggression

– Few genes identified

Reviewed in Holldobler & Wilson, The Ants, 1990

Semiochemical & Anatomy Ontology

• derives_from relationships need to be defined

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Linking Behavior, Anatomy, & Semiochemicals

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Present & Future work• Collection of terms & definition from honeybee and ant literature &

community

• Prioritization of behaviors associated to genes discovered in behavioral microarray experiments

• Curation of ‘derives_from’ relationships for semiochemicals and anatomy

• Curation of ‘precedes’ and ‘follows’ relationships for behavior actions (e.g. mating)

• Adaptation of Drosophila anatomy onotology for honeybees and ants

• Determination of cross-products with other ontologies such as CHEBI and GO

Ackowledgements• Drosophila Heterochromatin Genome Project (DHGP)

– Chris Mungall - Databases, Ontologies– Nicole Washington - PATO– Suzanna Lewis- Group Leader– John Richter - OBO-Edit

• Collaborators– Neil Tsutsui - UC Irvine

– Chris Elsik - BeeBase

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