Evolutionary significance of stochastic forces and small populations Coyne JA, Barton NH and Turelli M A critique of Sewall Wright’s shifting balance theory of evolution. Evolution 51:

Genetic differentiation Evidence for population differentiation in plants is indisputable. –Deterministic forces (Natural selection) –Stochastic processes (Genetic drift)

Drift causes random changes in allele frequencies Simulated population; N = 10

Determinants of drift small population size (N) restricted dispersal (m) N N N N N population neighbourhood

Effective population size, N e -a standardized measure of population size -size of an ‘idealized’ population with the same strength of genetic drift as the target population. - the census number (N), adjusted for skewed sex ratio, perenniality, selfing, persistent seed bank, ploidy, non-random variation in fecundity etc. - most cases, N e is less than the actual count of individuals in the population (N)

How important is chance? Darwin (1859): acknowledged that historical accidents and chance could oppose the forces of natural selection Gulick (1872): Hawaiian land snails Hagedoorn, A. L. and Hagedoom, A. C. The Relative Value of the Processes Causing Evolution. Pp Martinus Nijhoff. The Hague, 1921.

Wright and Fisher Fisher: adaptive evolution results simply from Darwinian mass selection. Wright: adaptation cannot be explained by selection alone. Stochastic processes such as genetic drift often play an important role.

Shifting Balance Theory Genotype/phenotype Fitness selection drift Fitness landscape selection

Coyne, Barton and Turelli 1997 “….it seems unreasonable to consider the shifting balance process as an important explanation for the evolution of adaptation”

Role of small populations and genetic drift in the evolution of mating systems in Eichhornia paniculata

Eichhornia paniculata Pontederiaceae short-lived perennial/annual insect pollinated Ephemeral water bodies in Brazil, Cuba, Jamaica, parts of Central America

3 mating types mating is disassortative and outcrossing stable state: frequency- dependent selection maintains equal morphs frequencies Tristyly

N = 167 populations Estimate mating type frequencies

Trimorphic = 118 Dimorphic = 42 Monomorphic = 7

Mating type structure Trimorphic populations near 1:1:1, or low on S Most dimorphic pops missing the S morph; All monomorphic pops are M

How is mating system measured? 1. Need 8-10 half sib offspring from each of mothers 2. Genotype mothers and offspring using genetic markers (allozymes, microsatellites, AFLPs) 3. Infer the genetic contribution of the paternal parent AB AA? AB Mother = AA 4. Estimate the rate of outcrossing (t) that produces the distribution of offspring observed. S = 1-t

Population outcrossing rate varies with mating type diversity Self-fertilizing 1 mating type Cross-fertilizing 3-mating types

Selfing variant of the M morph

Natural selection against the S morph, perhaps related to pollinator x mating type interactions Stochastic events associated with small, short- lived populations What evolutionary forces have caused the the loss of mating types and the transition from a stable outcrossing breeding system to self-fertilization? Hypotheses

Selection Pollinator limitation: long-tongued solitary bees; may be unpredictable in small pops; S morphs may be most vulnerable Fertility in the field but S < M,L in 3 of 6 pops F = 0.31, p > 0.50

Effective Population Size (N e ) Individual-based simulations of tristylous populations When N e < 40, drift can overcome selection and cause the loss of mating types. N e < 10, more likely to lose two mating types.

Mating types not lost equally S morph - most likely to be lost ssmmssMm ssMM SsMm SsMM SSMm SSMM frequency-dependent selection resists loss of morphs if 1:1:1, all morphs equally likely to disappear due to sampling error however, S allele is only carried by S morphs and thus cannot segregate from remaining L and M.

Effective population size in 10 populations of E. paniculata Genetic method Sample allele frequencies over at least 2 years Variance in allele freq. NeNe V(p) =

N e - Demographic method Five estimates 1.Estimate # of individuals 2.N, corrected for variation in among years 3.N, corrected for variance in flower production 4.N, corrected for mating type frequency 5.N, corrected for self-fertilization

NeNe Mean N = 763 (range ) Mean N e = 15.8 (range ) Mean N e / N = N e < 40 in 120 of 167 pops N e /N Demography Temporal var = 0.47 Reprod effort = 0.42 Selfing rate = 0.98 Morph freq = 0.95

Effect of drift on Spatial variation in morph structure Predictions Effective population size

Dimorphic/monomorphic Trimorphic Spatial variation in mating type structure

Temporal variation in frequency of S mating type S morph lost from pops

Temporal variation in S as a function of N

What accounts for the loss of the L morph? Reproductive assurance: ability to self-fertilize in the absence of pollinators favours selfing M morph F=2.8, p = 0.13

Why doesn’t the M morph spread in trimorphic populations? pollinators not scarce in large pops siring advantage doesn’t exist when S is present

Genotype/phenotype Fitness selection drift Fitness landscape selection outcrossing selfing