1. OdsH homeobox gene whose normal function within species involves enhancement of sperm production Drosophila simulans and D. mauritiana hs



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Table S1. Examples of genes causing intrinsic reproductive isolation (RI), and the extent to which they fit the three criteria for a ‘speciation gene’. HI = intrinsic hybrid inviability, HS = intrinsic hybrid sterility.

Gene

Details of gene and function within species

Study system

Form of RI

Criterion 1:

Gene affects RI1



Criterion 2:

Time of divergence2



Criterion 3: Effect size3

references

1. OdsH

Homeobox gene whose normal function within species involves enhancement of sperm production

Drosophila simulans and D. mauritiana

HS

1: Gene affects RI

(causes roughly 50% sterility; other nearby genes required to confer full hybrid sterility)



Unknown

(but likely not recent; OdsH reflects species boundaries more strongly than random loci)



Unknown

[S1-S4]

2. Xmrk2

Encodes a receptor tyrosine kinase that is overexpressed in some hybrids

Xiphophorus fish species (e.g. X. maculatus and X. helleri)

HI

1: Gene affects RI

(sometimes lethal tumorigenesis in hybrids or embryonic lethality)



Unknown

(species easily hybridized in lab)



Unknown

(effects on RI vary strongly among crosses)



[S5-S6]

3. Hmr

Encodes a protein with DNA-binding domains similar to some transcription factors, functional divergence between species shown

Drosophila simulans and D. melanogaster

HI, HS

1: Gene affects RI

(affects


viability and sterility and fertility, both sexes affected in some way)

Unknown

(but likely not recent; changes via positive selection occurred in the fairly distant past)



Unknown

[S7-S8]

4. Lhr

Functionally diverged in D. simulans and interacts

with Hmr to cause F1 HI, localizes to heterochromatic genomic regions



Drosophila simulans and D. melanogaster

HI

1: Gene affects RI

(contributes to lethality in F1 hybrid males, other genes might be involved in causing full lethality)



Unknown


Unknown


[S9]

5. Nup96

Encodes a nuclear pore protein

Drosophila simulans and D. melanogaster

HI

1: Gene affects RI

(explains complete hybrid lethality)



Unknown

(but likely not recent; changes via positive selection occurred in the fairly distant past)



Unknown


[S10]

6. Prdm9

Encodes a histone H3 lysine 4 trimethlytransfer-ase

Mus musculus house mouse subspecies

HS

1: Gene affects RI

(affects hybrid sterility)



Before complete RI

(RI between subspecies is known to be incomplete)



Large

(hybrid sterility effects are strong and RI via other barriers is incomplete)



[S11]

7. JYAlpha

On the 4th chromosome of

D. melanogaster but on the 3rd chromosome of D. simulans

Drosophila simulans and D. melanogaster

HS

1: Gene affects RI

(strong effects on hybrid male sterility)



Unknown

(but not recent; a relatively ancient gene transposition)



Unknown

[S12]

8. Overdrive

Causes segregation distortion in F1 hybrids as well as RI

Drosophila pseudoobscura subspecies

HS

1: Gene affects RI

(causes hybrid male sterility)



Before complete RI


Large

(as hybrid sterility effects are strong and RI due to other barriers is incomplete)



[S13]

9. Aep2

Mitochondrial protein encoded on chromosome 13, interacts with a mitochondrial gene to cause HS

Saccharomyces bayanus and S. cerevisiae yeast species

HS

1: Gene affects RI

(likely causes complete sterility)



Unknown

Unknown

[S14]

10. NB-LRR


Disease resistance gene homolog

Arabidopsis thaliana populations

HI

1: Gene affects RI

(affects hybrid necrosis)



Before complete RI

Large

(can cause severe HI and RI due to other barriers is incomplete)



[S15]

11. Nup160

Encodes a nuclear pore complex protein, and the protein encoded by Nup160 interacts with that of Nup96

Drosophila simulans and D. melanogaster

HI

1: Gene affects RI

(affects hybrid lethality)



Unknown;

(no evidence for recent selective sweeps)



Unknown

[S16]

12. PPR genes

Cluster of pentatricopeptide repeat genes, within a QTL for cytonuclear hybrid incompatibility

Mimulus guttatus and M. nasutus

HS

2: Gene associated with RI

Before complete RI; (hybrids frequently observed, molecular data show gene flow)

Unknown (QTL cause strong sterility, but prezygotic isolation is also strong)

[S17-S18]

13. cytc

A mitochondrial gene which interacts with nuclear genes to cause hybrid breakdown

Crosses between allopatric populations of Tigriopus californicus copepods

HI

2: Gene associated with RI

(but HI variable among crosses and environmental conditions)



Before complete RI

(causes RI in intraspecific crosses between populations)



Unknown

[S19-S20]

14. infertility QTL

QTL, genes not known

Lycopersicon esculentum and L. hirsutum

HS

4: Gene unknown, RI known

Unknown

Unknown

[S21]

1Criterion 1. Evidence that a gene affects RI. The four classes of evidence discussed in the text are evaluated. 1: Gene affects RI. Includes cases in which positional cloning, gene expression, gene knockout, phenotypic effects of mutations in the gene, or transgenics provide evidence that the gene in question causally affects RI. 2: Gene associated with RI. A known gene is associated with RI, but the genetic evidence is correlative such that another gene could be causing the association. 3: Gene known, RI only inferred. Strong evidence is available that a gene affects a phenotypic trait under divergent selection, but effects on RI are indirectly inferred from divergent selection. 4: Gene unknown, RI known. Reproductive isolation maps to a genomic region, but the specific gene(s) are yet to be identified.

2Criterion 2. Evidence that divergence in the gene occurred prior to the evolution of complete reproductive isolation. Before complete RI: Includes intraspecific comparisons and cases in which recurrent hybridization occurs between species. Not recent: Includes old species exhibiting complete reproductive isolation for which phylogenetic, population genetic or other analyses suggest divergence in the candidate speciation gene was not recent.

3Criterion 3. Effect size of the gene. Large: Includes cases in which contributions of the gene to current day reproductive isolation are detectable and considerable, and speciation is not yet complete.
Table S2. Examples of candidate speciation genes affecting forms of reproductive isolation other than intrinsic postmating isolation, with evidence for the three ‘speciation gene’ criteria summarized.

Gene

Details of gene or phenotype affected

Study system

Putative Form of RI

Criterion 1: Gene affecting RI

Criterion 2:

Timing of divergence



Criterion 3: Increase in total RI

references

1. OBP57d and OBP57e


Odorant binding proteins which affect test perception and host plant preference

D. melanogaster and D. sechellia (the latter has evolved distinct physiological and behavioral adaptations to a unique host plant)

DHP

1: Gene affects RI (affects host plant preference)

Unknown

Unknown


[S22]

2. Eda

Lateral plate number (in part, adaptation to predation regimes)

Gasterosteus aculeatus freshwater and marine stickleback fishes

II, EDHF

3: Gene known, RI only inferred

(some genetic evidence for divergent selection)



Before complete RI

(RI between marine and freshwater forms incomplete)



Unknown


[S23-S25]

3. Pitx1

Pelvic spine apparatus (in part, adaptation to predation regimes)

Gasterosteus aculeatus freshwater and marine stickleback fishes

II, EDHF

3: Gene known, RI only inferred

(effect on RI could be small)



Before complete RI

(as for Eda)



Unknown

[S26-S27]

4. Mc1r

Pigmentation (adaptation to be camouflaged against visual predation)

Peromyscus poliontos mainland and beach oldfield mouse subspecies

II, EDHF

3: Gene known, RI only inferred

(effect on RI could be small and effects on phenotype vary among traits)



Before complete RI

Unknown


[S28]

5. Agouti

Pigmentation (adaptation for crypsis via visual predation)

Peromyscus poliontos beach mouse subspecies

II, EDHF

3or 4: Gene associated with traits, linked genes could contribute, RI only inferred


Before complete RI

Unknown


[S29]

6. LWS Opsin

Vision (visual adaptation to different light environments)

Pundamilia pundamilia and P. nyererei cichlid fishes

II, EDHF, possibly DHP and SI

3: Gene known, RI only inferred

(but mixed experimental evidence for RI)



Before complete RI

(relatively common hybridization known)



Unknown


[S30]

7. ROSEA (also ELUTA, SULFUREA)

Flower color (attractiveness and adaptation to different pollinators)

Antirrhinum majus striatum and Antirrhinum m. pseudomajus flower morphs

II, EDHF

3: Gene known, RI only inferred


Before complete RI

(hybridization known)



Unknown

[S31]

8. Wingless

(QTL)

Mimetic wing color and mate preference

Heliconius cydno and H. pachinus mimetic butterflies

II, EDHF, SI

2: Gene associated with RI

(gene is within a QTL for RI)



Before complete RI

(hybridization known)



Unknown

[S32]

9. CDPK

(QTL)

Salt tolerance (adaptation to different soil salinities)

Helianthus sunflower species

II

2: Gene associated with RI

(gene is within a QTL for RI)



Unknown

Unknown

[S33]

10. Tpi

(QTL)

Perhaps diapause development timing differences

Pheromone and diapause races of Ostrinia nubilalis corn borers

TI

2: Gene associated with RI

(gene is within a QTL for RI)



Before complete RI

(hybridization known, see also Fig. 3)



Unknown

[S34]

11. Lysin

Sperm protein involved in fertilization

Haliotis rufescens and H. corrugata

abalone species



GI

2: Gene associated with RI

(but site-directed mutagenesis suggests causality)



Before complete RI

(hybridization in the wild known, but appears rare, indicating strong RI)



Unknown

[S35-S37]

12. Bindin

Sperm protein involved in fertilization

Echinometra mathaei populations, but also implicated in many other sea urchin taxa




2: Gene associated with RI


Before complete RI for E. mathaei populations (but unknown for other taxa, where hybridization appears very rare)

Unknown

[S36-S40]

13. Mc1r

Plumage color differences

Incipient species of Monarcha castaneiventris flycatchers

SI

2: Gene associated with RI


Before complete RI

Unknown


[S41-S42]

14. pgFAR

Pheromone production

Z and E pheromone races of Ostrinia nubilalis

SI

1: Gene affects RI (affects pheromones known to cause SI)

Before complete RI

Unknown

(other reproductive barriers do exist)



[S43]

15. YUP (QTL)

Flower color (attractiveness and adaptation to different pollinators)

Mimulus lewisii and M. cardinalis monkeyflower species

II, EDHF, PI

4: Gene unknown, RI known

Unknown

(RI is strong but incomplete, hybrids are fertile)



Unknown

(but see Box 1 for range of possibilities)




[S44-S46]

16. Pe and Pr (QTL)

Performance on (Pe) and preference for (Pr) different hosts plant species

Acyrthosiphon pisum host races on Alfalfa versus Clover

II, EDHF, DHP

4: Gene unknown, RI known

Before complete RI


Large

(as barriers other than Pe and Pr are weak)



[S47-S48]

17. Coy-2

(QTL)

Reinforced mating discrimination

D. pseudoobscura and its sibling species D. persimilis

SI

4: Gene unknown, RI known

(but 30 candidate genes reside within the QTL)



Before complete RI

(hybridization known)



Unknown

[S49]

18. Song and Preference

(QTL)

Male song and female acoustic preference for song

Laupala kohalensis and L. paranigra crickets

SI

4: Gene unknown, RI known


Unknown

Unknown

[S50]

19. X-linked gene (QTL)

Behavioral isolation via male behavior

Japan and Pacific ocean forms of Gasterosteus aculeatus stickleback fish

SI (also some effect on HS)

4: Gene unknown, RI known


Before complete RI

(hybridization known)



Unknown

[S51]

See Online Table 1 for explanations of criteria and categories. II = Immigrant Inviability (ecologically-based selection against migrants between environments), EDHF = ecologically-dependent hybrid fitness, PI = pollinator isolation (= sexual isolation in plants), SI = sexual isolation, DHP = divergent habitat preferences, which contribute to habitat isolation, TI = temporal isolation. GI = gametic isolation.

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S51 Kitano, J., et al. (2009) A role for a neo-sex chromosome in stickleback speciation. Nature 461, 1079-108
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