Laurie S. Stevison Suzanne E. McGaugh Mohamed A. F. Noor Why the association between interspecies divergence and inversions in Drosophila? Laurie S. Stevison Suzanne E. McGaugh Mohamed A. F. Noor

Recombination maintains cohesion of species Species are “groups of alleles in long-term association” – linkage disequilibrium Similar to some definitions of species Implicit in other definitions of species Stopping recombination maintains distinct (haplo)types

Chromosome inversions “prevent” recombination between types Problems with chromosomal pairing Single crossovers lead to acentric or dicentric chromosomes

Chromosome inversions “prevent” recombination between types Problems with chromosomal pairing Single crossovers lead to acentric or dicentric chromosomes Maybe help maintain species?

Test system: Drosophila pseudoobscura /D. persimilis Morphologically identical Hybrid females fertile (though males sterile) Overlapping range/ hybridize at low level Extensive genome sequence data

Inversions may have kept Drosophila pseudoobscura and D Inversions may have kept Drosophila pseudoobscura and D. persimilis apart >10 years of research summarized here: Genetic mapping of differences: Everything maps to 3 inverted regions Hybrid male sterility Mate preference Courtship song When studying nonhybridizing population, effects map outside inversions, too.

Inversions may have kept Drosophila pseudoobscura and D Inversions may have kept Drosophila pseudoobscura and D. persimilis apart Inverted regions show higher sequence difference than non-inverted regions Dpse-Dper looks like Dpse-Dpse when get >2.5Mb from inversion

Inversions may have kept Drosophila pseudoobscura and D Inversions may have kept Drosophila pseudoobscura and D. persimilis apart Yellow: inverted regions Blue: collinear regions Complete suppression of recombination products until ~2.5 megabases outside inversion Within species, 2.5 megabases would experience >10% recombination

Inversions may have kept Drosophila pseudoobscura and D Inversions may have kept Drosophila pseudoobscura and D. persimilis apart! Trait differences map to inverted regions in hybridizing populations Don’t see similar association in non-hybridizing populations Higher differentiation in inverted than non-inverted regions Domain of effect of inverted region matches domain of effect on recombination So… are we done? One fly in the ointment…

Simulation study raises questions… Inversions don’t completely stop gene flow Do get double-crossover or gene conversion exchange in inverted region Over long time, low gene flow often erodes sequence differences within inverted regions Figure is one of the “best” case-scenarios

Conclusions… “the low levels of recombination within an inversion often result in the loss of accentuated divergence in inverted regions compared to collinear ones” (2009) “the effects of chromosomal rearrangements can be transient and will be quantitative and not qualitative” (Feder et al 2011)

Model Results ≠ Experimental Results Model says unlikely to see (sustained) difference in inverted region Data show difference associated with inverted region and no indication that sympatry is very recent Both are “right”– what’s up?

Some explanations suggested by Feder & Nosil More exchange in center than near breakpoints Inversion association stems from breakpoint areas Clustering of loci within some regions Very recent secondary contact/ gene flow Mapping ascertainment bias Mixed geographic mode of speciation may help

Study a matching intra- and inter-species inversion difference!

What MIGHT we find? A<B because B linked to inversion D<C if have “double crossovers” in center of inverted region In hybrids, ~1/10,000 progeny have double crossovers (L. Stevison)

What do we find? Interspecies A << B ≤ D ≤ C Regions far outside inversion (A) have low sequence divergence All regions near or within inversion (B, C, D) have high sequence divergence

What do we find? Intraspecies A ≤ B ≤ D << C Regions near inversion but inside (C) have high divergence All regions far, near, or centrally within inversion (A, B, D) low

Intraspecies and Interspecies patterns differ… Divergence Divergence

Intraspecies and Interspecies patterns differ… Effects of “rare events” cause difference? BOTH: Rare double-crossovers (10-5) BOTH: Low crossover rate just outside inversion (10-5?) INTER: Low rate of hybridization (10-5)

Interaction of hybridization and recombination rates matters! WITHIN SPECIES– Rare exchanges in center and outside breakpoint make little divergence persist Fits model: recombination rate even higher, 10-5, but that was “maximum” in center of largest inversion BETWEEN SPECIES– Rare exchanges x rare hybridization allows divergence to persist even in areas of low (but non-zero) recombination Exchange rate low: 10-5 x 10-5 = 10-10

Resolution Inversions were important in the persistence of Drosophila pseudoobscura & D. persimilis Possible reason for high divergence persisting in inverted regions is migration rate extremely low: rare2 effect Importance of descriptive natural history Relied on pre-1985 field estimates of hybridization rate to get to this important conclusion

Punchline: efficacy of inversions in allowing hybridizing species to persist is affected by hybridization rate: - If high, inversion effect decays - If low, inversion effect persists Thank you!