Natural Selection I:

1. Natural Selection I: Artificial Selection

2. Darwin and fancy pigeons • Analogy between artificial and natural selection central to the Origin • If humans can produce such divergent phenotypes in short time periods through selection (as in pigeons) wouldn’t nature be able to produce the same over millions of years of natural selection? • Darwin discusses products of domestication: cows, rabbits, sheep Secord 1981

3. Jacobin English Carriers http://members.aol.com/duiven/highlight/jacobin/yelljac.jpg Fantail Pouter http://pages.britishlibrary.net Runt http://www.yp-connect.net/~poultry/3af1caa0.jpg http://www.yp-connect.net/~poultry/39a2cc30.jpg http://members.aol.com/duiven/highlight/king/runtw.jpg

4. A common origin? The Rock Pigeon Columba livia “Great as the differences are between the breeds of pigeons, I am fully convinced that the common opinion of naturalists is correct, namely that all have descended from the rock-pigeon.” http://www.samford.edu/schools/artsci/biology/vert-zoo-04s/photos/Columba-livia.jpg

5. A common origin? Secord 1981 • Classification methods relied on traditional characters (mainly the beak) • Tumblers were grouped together, but the affinities with the other short-beaked pigeons unknown (third group artificial)

6. A common origin? • If fancy types were produced by crossing, the number of wild progenitors would at least be 7 or 8, most of which would be extinct • None of the domesticated forms have returned to their natural state, as would be expected if close to their wild progenitors • The ancestral species would have to be capable of domestication, an unusual property • If the distinct ancestral species had existed originally, men would have chosen a very strangely modified set of birds, different from all existing members of the family • All the domestic pigeons can be intercrossed, producing fertile offspring • The fancy pigeons bear a fundamental similarity to the rock pigeon-both in habits and general structure-that they share with no other bird

7. A common origin? Secord 1981 • Why was a priority of Darwin’s to establish a common ancestry for fancy pigeons? • Is common ancestry necessary to strengthen his arguments of natural selection?

8. The process of selection The fancier was the selecting agent itself, who could impose two principal types of selection: 1. Methodical selection 2. Unconscious selection What was Darwin’s reason for differentiating the two? Secord 1981

9. Artificial selection as an analogy The argument that artificial selection is analogous to natural selection is a key component of the Origin of Species, The Descent of Man, and Variation of Animals and Plants Under Domestication • Darwin’s artificial selection analogy argued by many historians and philosophers as just an analogy to aid in explaining the parallels with natural selection

10. Artificial selection as an analogy The argument that artificial selection is analogous to natural selection is a key component of the Origin of Species, The Descent of Man, and Variation of Animals and Plants Under Domestication • Wilner (2006) argues artificial selection should be conceived as a multifaceted experiment. • Traditional experiment: lead to theories of natural selection. • Non-traditional: disclosed the nature of hereditary variation

11. Darwin’s hopeful monsters Darwin frequently referred to the results of artificial selection as “monstrous” • Many portray this as an indication of the irrelevance of artificial selection to natural phenomena http://www.dailymail.co.uk

12. Darwin’s hopeful monsters “The circumstances under which our domestic productions are reared are widely different. . . In conformity with this, all our domesticated productions, with the rarest exceptions, vary far more than natural species.” -Darwin (1896) Wilner (2006) views Darwin’s use of “monstrous” in an experimental sense. Darwin’s “monstrous” refers to the degree of artificiality in the breeders’ experiment. Experiments uncover the nature of the elements, often with very artificial treatments.

13. Is artificial selection analogous to natural selection? • Does artificial selection mimic natural selection to any degree? • Degree of selection pressure • Methodical vs unintentional selection • Convergent evolution • What would be concrete evidence?

14. Crop Domestication Doebley et al. In Press • Multiple different independent centers of domestication • Selective breeding of wild plants and animals began 10,000 years ago

15. Crop Domestication • Most researchers believe agriculture began as an attempt to modify the landscape and encourage growth of edible wild plants • Key to domestication would be a switch from letting wild edible plants to naturally re-sow themselves in burned field, to sowing seed from previous season • Does this early form of breeding constitute an unconscious selection regime? Doebley et al. In press.

16. Crop Domestication • Widely viewed that early artificial selection of crops would have been largely unintentional • Farmers, for instance, would collect seeds that had not shattered and fallen to the ground • The non-shattering allele frequency would rise in the population • Similar selection thought to occur for seed dormancy, synchronous flowering, increased apical dominance, and larger seeds Doebley et al. In press.

17. Genetic bottlenecks in domestication • Genetic bottlenecks reduce genetic diversity, which have implications for further breeding • Loci that are targets of domestication can have signatures of selection: nucleotide diversity can be even lower than neutral genes Doebley et al. In press. Do these genetic bottlenecks in domestication reflect natural systems of selection?

18. Candidate genes in domestication • teosinte branched 1 • Teosinte highly branched • Maize has one dominant axis of growth, axillary branches are short and feminized • Signature of selection confined to upstream promoter region Hubbard et al. 2002

19. Candidate genes in domestication • teosinte glume architecture 1 • SBP-family of transcriptional regulators • 7 fixed differences within a 1kb region between teosinte and maize • 1 in coding region, others potentially affect regulation Wang et al. 2005

20. Candidate genes in domestication Many genes implicated in domestication are shown to be involved in gene regulation or in regulatory regions themselves. Does this follow a similar pattern to natural systems? • Signatures of positive selection show the a cauliflower gene carrying a nonsense mutation is segregating in broccoli, wild cabbage, kale, and cauliflower. A floral regulatory locus

21. Candidate genes in domestication • Inflorescences of maize, unlike those of related grasses lack long branches • Maize ramosa1 gene controls inflorescence architecture • ra1 has a signature of positive directional selection • Similar patterns in natural species, Micanthus sirensis and Sorghum bicolor Vollbrecht et al. 2005

22. Candidate genes in domestication • Inflorescences of maize, unlike those of related grasses lack long branches • Maize ramosa1 gene controls inflorescence architecture • ra1 has a signature of positive directional selection • Similar patterns in natural species, Micanthus sirensis and Sorghum bicolor Vollbrecht et al. 2005

23. Developmental constraint in dog domestication • Multiple origins of dogs from wolves greater than 14,000 years ago with repeated genetic exchange between dog and wolf populations • Metrics describing aspects of canine skeletal morphology extracted from X rays and DNA • Principal component analysis • Skull and limb lengths inversely correlated with the strength of the limb and axial skeletons Parker and Ostrander 2005

24. Convergent evolution in dog domestication • Dogs can read human communicative gestures (ie.pointing) better in comparison than wolves • Unclear if this ability is a result of direct selection or a by-product of selection against fear and aggression towards humans • Experimental population of fox kits bred over 45 years to approach humans fearlessly and non-aggressively • As skillful as dog puppies in human gestures and more skillful than a second control population of fox kits

25. Experimental evolution in E. coli • >30,000 generations starting from a clonal line • Serial transfer regime, populations diluted 1:100 each day into 10ml • 6.6 generations per day • Homogeneous environment • Replicate populations • Samples from each generation stored for further genetic analysis http://www.msu.edu/~lenski/photoinlab.jpg

26. Experimental evolution in E. coli • “We emphasize that our experiments employ natural selection, and not artificial selection as practiced by breeders and many experimentalists” • True? http://www.msu.edu/~lenski/photoinlab.jpg

27. Experimental evolution in E. coli Cell Volume Lenski and Travisano 1994 http://commtechlab.msu.edu/sites/dlc-me/zoo/Pf07002.jpg

28. Experimental evolution in E. coli Fitness Lenski and Travisano 1994 Is this a traditional or non-traditional experiment?

29. Experimental evolution in E. coli • Other findings: • Pleiotropic effects of fitness mutations. Both postitive and negative. • Two ecologically and morphologically distinct types evolved: L and S by generation 6,000 and persisted for more than 12,000 generations after. Phylogenetic analysis of over 200 clones indicates that S was monophyletic. Fitness experiments indicate both lineages continued to evolve which contributed to their general frequencies over time. Different species. • Parallel changes in DNA topology between populations. Mutations in topA and fis, which control DNA supercoiling. • Parallel changes in gene expression from growth in a glucose-limited medium. Expression of 59 genes had changed significantly in the same direction in two selected populations. A mutation in a regulator spoT produced many of these expression differences.

30. Experimental evolution in E. coli • Some mutation facts about E. coli: • After 10,000 generations, each pop. Underwent 7.5 X 1011 replications • Mutation rate: 2.5 X 10-3 mutations per genome replication • Each pop. Experienced 2 X 109 mutations • With 5 X106 bp per genome and three alternative point mutations at each bp, this translates to >100 occurrences of every point mutation in the whole genome

31. Conclusions Is artificial selection analogous to natural selection? Can artificial selection be used as evidence for evolution?

32. References Doebley, J.F., Gaut, B.S., Smith, B.D. In press. The molecular genetics of crop domestication. Evans, L.T. 1984. Darwin’s use of the analogy between artificial and natural selection. Journal of the History of Biology. 17: 113-140. Gould, S.J. 1991. What the immaculate pigeon teaches the burdened mind. Natural History. 100: 12-21. Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., Trut, L. 2005. Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol. 15: 226-230. Hubbard, L., McSteen, jP., Doebley, J., and Hake, S. 2002. Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and tewosinte. Genetics. 162: 1927-1935. Lenski, R. and Travisano, M. 1994. Dyanmics of adaptation and diversification: A 10,000 generation experiment with bacterial populations. Proc. Natl. Acad. Sci USA. 91: 6808-6814. Parker, H.G. and Ostrander, E.A. 2005. Canine genomics and genetics: running with the pack. PLOS. 1: 507-513. Purugganan, M.D., Boyles, A.L., Suddith, J.I. 2000. Variation and selection at the cauliflower florwal homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetcs. 155:855-862. Ruse, M. 1975. Charles darwin and artificial selection. J. Hist. Ideas. 36: 339-350. Secord, J.A. 1981. Nature’s fancy: Charles Darwin and the breeding of pigeons. ISIS. 72: 163-186. Vilà, C., Savolainen, P., Maldonado, J.E., Amorin, I.R., Rice, J.E. Honeycutt, R.L., Crandall, K.A., Lundeberg, J., Wayne, R.K. 1997. Science. 276: 1687-1689. Vollbrecht, E. and Sigmon, B. 2005. Amazing grass: developmental genetics of maize domestication. Biochemical Society Transactions. 33: 1502-1506. Vollbrecht, E., Springer, P.S., Goh, L., Buckler, E.S. IV, Martienssen, R. 2005. Architecture of floral branch systems in maize and related grasses. Nature. 436: 1119-1126. Wang, H., Nussbaum-Wagler, T., Li, B., Zhao, Q., Vigourous, Y., Faller, M., Bomblies, K., Lukens, L., Doelbey, J. 2005. The origin of naked grans of maize. Nature. 436: 714-719. Wilner, E. 2006. Darwin’s artificial selection as an experiment. Stud Hist Philos Biol Biomed Sci. 37: 26-40. Wright, S.I., Bi, I.V., Schroeder, S.G., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S. 2005. The effects of artificial selection on the maize genome. Science. 308: 1310-1314.