1. Post-zygotic isolation results when hybrid offspring are: - inviable (fail to develop at all) - viable, but infertile (one or both sexes cannot reproduce) Hybrid breakdown is the term for infertility in viable hybrids - many hybrids, like mules, are viable but cannot reproduce - often results from male sterility (failure to make sperm, etc) - hybrids can sometimes backcross with a parent species Post-zygotic reproductive isolation

2. 1 st generation (F1) hybrids are often viable (= they live just fine) because they have inherited one co-adapted gene complex from each set of parental chromosomes Post-zygotic isolation: hybrid breakdown maternal proteins all fit together and interact paternal proteins all fit together and interact

3. When hybrid offspring reproduce, independent assortment assures that they will not pass on co-adapted gene complexes - their offspring get a mix of genes that are not adapted to fit together, so they don’t form working protein complexes Result: hybrids cannot produce F2 offspring if their parents were too distantly related Post-zygotic isolation: hybrid breakdown

4. Haldane’s Rule: usually the heterogametic sex is sterile or inviable in the F1 generation of hybrids - XY for mammals, flies (male) - WZ for birds, butterflies (female) Female mammals have one complete set of genes from maternal X, and one from paternal X chromosome - can produce needed proteins to interact with rest of maternal and paternal chromosomes Males only have an X from mom; cannot supply X-linked gene products needed to interact with rest of dad’s genome - are unable to make reproductive protein complexes needed for spermatogenesis (sperm-making) Post-zygotic isolation: Haldane’s Rule

5. Molecular data indicate that genes under positive selection are commonly involved in post-zygotic isolation - genes that have partner-proteins, and rapidly evolve changes in their respective amino acid sequences, cause problems when species hybridize - the protein-partners of different species don’t fit together Post-zygotic isolation & Positive selection

6. Example: the Nup160 gene codes for part of the Drosophila nuclear pore protein complex - Nup96 and Nup160 alleles from D. simulans are lethal when combined with some X-linked gene in D. melanogaster - both genes evolved under strong positive selection, and are now so different from D. melanogaster alleles that they are fatal when combined with their partner proteins from melanogaster Post-zygotic isolation & Positive selection

7. In some cases, hybrids may produce offspring that are fertile, at least when they backcross with one of their parental species - hybrids may have same or even higher fitness than parents (if alleles interact favorably in a certain combination, or ecological circumstances are juuuust right) - documented among plants, birds Sometimes, key alleles can be introduced to a species through hybridization + back-crossing to one of the parental species - introgression: alleles move from one species into another - documented in Darwin’s finches Viable hybrids as a source of genetic variation

8. Rare but important hybridization events have been documented during a 30-year study of Darwin’s finches (several species) One case: 2 small G. fortis females mated with scandens males - male offspring imprinted on paternal songs, bred back into scandens population (which was only ~200 birds) Introgression resulted because hybrids were able to breed back into one of the parental populations - re-introduced alleles that had been lost from G. scandens during the speciation process why were male hybrids able to backcross in these birds?.. Introgressive hybridization in Darwin’s finches

9. Because fortis is much smaller, the mean beak size of the scandens population went way down in the following years - introduction of alleles from fortis strongly affected the genetic makeup of the scandens population White bars show the large negative change in beak size, due to hybrid offspring in the population 20011972

10. In some plants, hybrids become their own species, genetically distinct from both parents and viable In animals, hybridization may result in what appear to be independent species - however, if the hybrids cannot produce offspring among themselves, they are not a true species in their own right Sometimes hybrids are mistaken for a true species due to a distinct morphology, different from either parent species Hybridization and species formation

11. As many as 105 coral species may simultaneously spawn on a single night over the same reef - despite obvious potential for hybridization, species remain distinct (no blurring of species boundaries) Are morphologically different corals really species, or just unrecognized hybrids? Vollmer and Palumbi studied 3 corals in the genus Acropora A. cervicornis, which lives on the back reefsibling A. palmata, which lives on wave-swept reef topsspecies A. prolifera, which has two growth forms: bushy and palmate Hybridization and coral reef diversity

12. 3 overlapping species of Acropora coral the two growth morphs of A. prolifera “bushy” morph“palmate” morph A. cervicornisA. palmata

13. Hybridization and coral reef diversity A. cervicornis A. palmata A. prolifera Different alleles fixed between cervicornis and palmata prolifera were all heterozygotes  they were...?

14. Mitochondria are only inherited from your mother - mitochondrial DNA haplotypes are maternally inherited “Bushy” morphs of A. prolifera all had mitochondrial DNA sequences that matched A. palmate sequences - thus, bushy prolifera corals are hybrids where the egg came from A. palmata colony and the sperm from A. cervicornis “Palmate” morphs of A. prolifera all had mitochondrial DNA sequences from A. cervicornis - the reverse case: palmate prolifera are hybrids where egg came from cervicornis and the sperm from palmata Hybridization and coral reef diversity

15. Implications: (1) Because corals are colonies that grow new polyps asexually, prolifera colonies may be “immortal mules” - ecological persistence of diverse morphologies (2) Coral reef “diversity” may actually reflect the presence of long-lived hybrids that have little evolutionary potential (3) Provides the opportunity for rare backcrossing with one of the two parent species  Hybridization and coral reef diversity

16. Conservation effort was underway to save the red wolf Encroaching coyotes were breeding with wild red wolves, and the species was disappearing 14 remaining individuals were caught and a captive breeding program established Then, geneticists at UCLA proved that the red wolf was actually a hybrid of grey wolves and coyotes - not a distinct species at all ! Hybrids and the Case of the Red Wolf

17. Hybrid Speciation Although common in plants, the formation of new species via hybridization is rare among animals For hybrid speciation to occur, hybrids must: 1) be viable and fertile 2) occupy a hybrid-specific ecological niche - otherwise, will be out-competed by a better-adapted parental species 3) quickly become reproductively isolated - otherwise, just serve as a vehicle for introgression between two parental species; won’t become their own lineage

18. 2 butterfly species occur on either side of Sierras - east, Lycaeides melissa; west, L. idas - species are sympatric across part of their ranges, where they live mid-way up the mountains - 3 rd form lives on top of mountains, above the tree line: “alpine” form Gompert et al. Science 2006 Hybrid speciation in Lycaeides butterflies

19. genetic studies revealed alpine butterflies are a distinct species with a mixed genome - a combination of L. melissa and L. idas Hybrid speciation in Lycaeides butterflies

20. Two species of butterflies occur on either side of the Sierras - east, Lycaeides melissa; west, L. idas - genetic data: alpine butterflies are a distinct species with a mixed genome, combining alleles of L. melissa + L. idas  alpine form evolved from a hybrid of the 2 parent species - alpine species no longer exchanges alleles with either parent species - reproductive isolation comes from at least 4 different sources...

21. A) alpine species is highly loyal to one host plant; others aren’t B) alpines lay non-sticky eggs that fall off leaves of host plant; other species glue eggs to leaves - on mountaintops, winds blow leaves away in winter so the non-glueing strategy is adaptive (gluers have low fitness) C) alpine butterflies have different color patterns on their wings used in mate signaling D) differences in male genital morphology

22. Case 2: Hybrid speciation by host-shift in Rhagoletis Schwarz et al. Nature 2005 R. mendaxR. zephyria honeysuckle fly blueberry maggot fly snowberry maggot fly - new fly race found on introduced honeysuckle plant - genetically a hybrid, with a mixture of alleles that are fixed in two parental races (blueberry + snowberry flies) - honeysuckle flies are not F1 hybrids - no excess heterozygotes

23. Speciation by hybridization.. plus some Among Darwin’s finches on island Daphne Major... - immigration from other islands is rare: -- 2 G. fortis and 1 hybrid over 18 yr -- 1 G. scandens over 24 yr - hybridization is rare: 13 fortis-scandens hybrids in 21 yr Mating choice is based on 2 things: - song that males sing; learned culturally from their dad - beak shape and size

24. In 1981, a hybrid immigrant arrived on Daphne and mated with a resident female, daughter of a hybrid-fortis backcross - both parents carried some scandens alleles - immigrant male was unusually large (had a big beak) - immigrant male sang his own weird song that didn’t match any existing finch songs - he came up with a strange, personal variant not sung by either species on any island... Grant & Grant, 2009, Proc Nat Acad Sci USA

25. In 1981, a hybrid immigrant arrived on Daphne and mated with a resident female, daughter of a hybrid-fortis backcross Only 2 of their great-great-grandkids survived a 2004 drought - boy and girl, who mated and started a highly inbred family line that only mated within itself for 3 generations (and counting..) This lineage is reproductively isolated from native G. fortis by two forms of pre-zygotic reproductive isolation - unique song sons learn from dad, to which girls respond - unusually large beaks, which make them look different from native fortis – a form of size-assortative mating

26. typical fortis immigrant lineage females of immigrant lineage prefer males who sing the funky song of their great-great-granddad, and who have freakishly big beaks Grant & Grant, 2009, Proc Nat Acad Sci USA

27. Summary: evolutionary importance of hybrids Hybrid lineage persists and is still reproductively isolated – case of incipient speciation due to hybridization, plus... - hybrid had exceptional size, due to scandens alleles (a bigger species – result of natural selection) - by immigrating his first year, that hybrid evidently came up with a screwy song all of his own (random event) - song transmission from father to son  new song lasted as long as some females responded to it (sexual selection) - following drought, only 2 large-beaked descendents left on island, who were siblings (bottleneck + inbreeding)

28. Summary: evolutionary importance of hybrids (1) When hybrids have lower fitness than either parent, selection will favor pre-zygotic isolation to prevent hybridization - parents who don’t produce low-fitness offspring have the highest fitness (2) Hybrids are often viable but sterile, owing to breakdown of co-adapted gene complexes in the F2 generation (3) Persistent hybridization or long-lived hybrids may cause intermediate phenotypes mistaken for distinct species (4) In hybrid introgression, alleles move between species 