Tate Holbrook ASU CSDC RiC

1. Putting theory into practice: empirical studies of group selection Tate Holbrook ASU CSDC RiC

2. What is group selection? • Group selection – differential survival and/or reproduction of groups; Cov(group-level phenotype, fitness) • Possible mechanism for evolution of social behaviors (inc. altruism), but applies to any trait that affects survival, dispersion, and/or colonization • Between-group genetic variance required for response • Relatedness is one of several potential sources • Multilevel selection – simultaneous at multiple levels (e.g., individual, group), in same or opposite directions • Mathematically equivalent to gene selectionism/inclusive fitness, but explicitly examines the components of evolutionary change in structured populations

3. The quantitative genetics perspective R = h2S S= selection differential = change in mean phenotype of population due to selection within generation = Cov(phenotype, fitness) R=response to selection = change in mean phenotype of population between generations h2 =heritability = proportion of phenotypic variance that contributes to response • Types of genetic effects Direct – individual phenotype influenced directly by genotype Indirect – individual phenotype influenced by expression of genes in interacting individual(s) * only group selection acts efficiently on genetic components arising from social interactions

4. How effective is group selection at producing an evolutionary response? • Is the ecological process of group selection common and strong in nature? Goodnight and Stevens 1997

5. Goodnight and Stevens 1997

6. Group selection for increased and decreased population size (i.e., mean productivity) • Control – individual selection • Rapid response to high and low group selection • Individual selection resulted in decreased population size • Changes in cannibalism rates, fecundity, development time

7. Poultry Science 1996 • Hens individually-selected for egg production are more aggressive, increase mortality and reduce overall production in multiple-hen cages • Selection among cages for increased egg production resulted in 60% increase in annual egg production per hen, compared to unselected controls • fewer aggressive interactions • lower mortality • worth $3 million!

8. “Wrinkly spreader (WS)” strain of Pseudomonas fluorescens evolves in response to anoxic conditions in unmixed liquid by producing a cellulosic polymer that forms mat on surface • Polymer is expensive – nonproducing “cheaters” have higher relative fitness within group, but as they spread, the mat deteriorates and sinks to bottom • WS is maintained by between-group selection despite selective disadvantage within groups Nature 2003

9. Metapopulations of bacterial host (E. coli) and phage (T4) cultured in 96-well plates • Different migration schemes executed by high-throughput liquid-handling robot • Spatially restricted migration favored ‘prudent’ phage strains over more ‘rapacious’ strains, which were prone to extinction

10. PNAS • Selection of soil ecosystems for above-ground biomass and aquatic ecosystems for pH • Phenotypes result from interactions among species and physical environment • Lab microcosms colonized by thousands of species, millions of individuals from single, well-mixed source • Sustained response to selection in 2 out of 3 experiments • Applications in bioremediation

11. Summary of lab experiments • Artificial group selection can produce evolutionary response • Same or opposite direction as individual selection • Group-selected phenotypes influenced by direct and indirect genetic effects • Genetic effects arising from social interactions can contribute to response to group selection, but not to individual selection

12. How effective is group selection at producing an evolutionary response? • Is the ecological process of group selection common and strong in nature? Goodnight and Stevens 1997

13. Measuring group selection in nature • Contextual analysis – multiple regression • Dependent variable: fitness component • Independent variables: individual and contextual (group-level) traits • Detects individual and group selection differentials (S), but cannot predict response to selection (R) – depends on heritability of traits

14. Goodnight and Stevens 1997

15. No queens • “Workers” reproduce parthenogenetically, forage when old • Large workers have more developed ovaries, less likely to forage • Measured relative individual fitness within colonies and mean individual lifetime reproductive success of colonies

16. Tsuji 1995: Results • Contextual analysis revealed conflicting selection • Individual selection (within-colony) for large workers • Group selection (between-colony) for higher proportion of small workers (foragers) • Response to selection depends on underlying genetics (?)

17. “Almost all the spectacular evolutionary efflorescence of the more than 12,000 known ant species, hence almost all the progressive advance of their communication and caste systems, life cycles, algorithms of colonial self-organization and caste-specific adaptive demographies, are manifestly the product of group selection acting on the emergent, colony-level traits, which are produced in turn by the interaction of the colony members.” - D.S. Wilson and E.O. Wilson 2007 © Alex Wild

18. “The challenge to theoretical biology is to incorporate nonadditive [indirect; associative] gene effects into models of multilevel selection. The challenge to empirical biology is to continue to document multilevel selection in natural populations, determine how frequently contextual traits influence fitness, and quantify the role of group selection in nature.” - Goodnight and Stevens 1995