Topic 8. Lecture 14. Direct observations of past evolution

1. Topic 8. Lecture 14. Direct observations of past evolution This topic can be viewed as a bridge connecting studies of past evolution and of Microevolution. Obviously, we cannot directly observe Macroevolution, because it is too slow, but even what can be observed is fascinating. We will treat the notion "direct observations" broadly and consider the following subjects: 1. Domestication 2. Selection experiments 3. Evolution of captive populations 4. Rapid evolution in the wild 5. Rapid evolution of human pathogens

2. 1. Domestication Not too many species of animals and plants were domesticated long time ago and underwent substantial changes under artificial selection. A. Goldfish The wild progenitor of domesticated goldfish Carassius auratus is a very common species in Eurasia.

3. A brief history of goldfish domestication During the Tang Dynasty (618 - 907), it was popular to raise Carassius auratus in ponds. As the result of a dominant mutation, one of these fishes displayed "gold" (actually yellowish orange) coloration. In 1162, the empress of the Song Dynasty (960 - 1279) ordered the building of a pond to collect the red and gold variety. The occurrence of other colors was first recorded in 1276. The first occurrence of fancy tailed goldfish was recorded in the Ming dynasty (1368 - 1644). Obviously, strong artificial selection was applied to external morphology and color of domestic goldfish, usually in the direction opposite to that of natural selection.

4. A small sample of breeds of goldfish, starting from less derived ones:

5. None of these fishes would do well in the wild. Genetic variation on which artificial selection operated was partially present in the wild progenitor population and partially provided by new mutations in captivity. These patterns are typical for all domestic breeds.

6. B. Pigeon The wild progenitor of domestic pigeon breeds, the Rock Pigeon has its native range in western and southern Europe, North Africa, and into southwest Asia. Its habitat is natural cliffs, usually on coasts. Rock Pigeons have been domesticated for several thousand years.

7. Darwin was an accomplished pigeon fancier: Believing that it is always best to study some special group, I have, after deliberation, taken up domestic pigeons. I have kept every breed which I could purchase or obtain, and have been most kindly favored with skins from several quarters of the world, more especially by the Hon. W. Elliot from India, and by the Hon. C. Murray from Persia. I do not believe that any ornithologist would ... place the English carrier, the short-faced tumbler, the runt, the barb, pouter, and fantail in the same genus. Great as are the differences between the breeds of the pigeon, I am fully convinced that the common opinion of naturalists is correct, namely, that all are descended from the Rock Pigeon (Columba livia). ("Origin of Species", 1859, Chapter 1)

8. A small sample of breeds of domestic pigeon:

11. "Semi-wild" pigeons that live alongside humans are polymorphic, as some of them are wild-type and others have dark plumage (melanists). In rural habitats, the wild type is prevalent, but in big cities dark individuals are more common.

12. C. Dog East Asian form of wolf, Canis lupus, the progenitor of domestic dogs.

13. A small sample of dog breeds:

14. A brief history of dog domestication Archaeological finds from Mesolithic sites around the world indicate that the dog was the first domestic animal. The earliest finds believed to be from domestic dogs are a single jaw from 14,000 years before the present in Germany and an assemblage of small canids from 12,000 yr B.P. in Israel. Genetic data firmly establish wolves as wild progenitor of dogs. Examination of the mitochondrial DNA sequence variation among 654 domestic dogs representing all major dog populations worldwide suggest a common origin from a single gene pool for all dog populations. A larger genetic variation in East Asia suggests an East Asian origin for the domestic dog, ~15,000 years ago.

15. Phylogenetic tree of all dog (unlabeled) and wolf (open squares) haplotypes. Six clades (A to F) of dog haplotypes are indicated. Branch lengths are according to the indicated scale; the branch leading to the outgroup (coyote) was reduced by 50%.

16. D. Experimental domestication of the fox, Vulpes vulpes wild foxes Domesticated foxes after 40+ generations of selection for tame behavior. (J. of Heredity 95, 185–194, 2004).

17. The story of fox domestication: The silver fox, a color variation of the red fox (Vulpes vulpes), has been domesticated in an experiment at the Institute of Cytology and Genetics in Novosibirsk. Starting in 1959, and selected solely on behavioral criteria, a strain of foxes with behavior extremely similar to domestic dogs was produced. A host of additional changes never deliberately selected for also appeared. They included piebald coat color, drooping ears, shorter, occasionally upturned tails, shortened snouts and shifts in the developmental timing of various other characteristics. The Fox-Farm experiment conclusively demonstrated that consistent and prolonged selection for a single behavioral trait can radically alter not only the behavior and developmental characteristics of an animal, but its physical constitution as well.

18. General patterns in animal domestication Several phenotypic traits appear independently in many domesticated animals. Usually, more than one substantially different genetic lineages of the wild progenitor is incorporated into domesticated breeds, indicating multiple domestication events (J. of Zoology 269, 261-271, 2006).

19. E. Domestication of maize, Zea mays. Annual teosinte, the wild progenitor of maize. The photograph shows the robust vegetative habit and long branches with tassels at their tips.

20. The history of maize domestication: Teosinte plants are taller and broader-leaved than most grasses. Their general growth form is similar to that of maize, although they have much longer lateral branches. Phylogenetic analysis indicates that one form of teosinte, known as Z. mays ssp. parviglumis, shares a particularly close relationship with maize and is its direct ancestor. A single domestication event that produced maize can be pinpointed to a specific geographic locality. Populations of teosinte from the central Balsas River drainage are basal to diversity of domestic maize, suggesting that this regions was the cradle of maize domestication. From the know rate of evolution of traits used for the phylogenetic reconstruction (microsatellite alleles), the time of divergence ssp. parviglumis and Mexican maize can be estimated as 5,700-13,100 B.P. Domesticated varieties of potato also originated monophyletically in the northern Peru, from a wild tuber-bearing Solanum.

21. Geographic distribution of maize and teosinte used for the phylogenetic analysis of maize domestication. Inset shows the distribution of the 34 populations of ssp. parviglumis in southern Mexico with the populations that are basal to maize. The blue line is the Balsas River and its major tributaries.

22. Phylogenies of maize and teosinte based on 99 microsatellites. Dashed gray line circumscribes the monophyletic domestic maize lineage. Asterisks identify those populations of ssp. parviglumis basal to maize, all of which are from the central Balsas River drainage. The arrow indicates the position of Oaxacan highland maize that is basal to all of the other maize.

23. Genetics of maize domestication A substantial portion of the phenotypic differences between maize and teosinte is explained by variation in an enhancer of gene expression at the tb1 (teosinte branched 1) locus. Intergenic sequences 58-69 kb 5' to the tb1 coding region confer pleiotropic effects on Z. mays morphology.

24. A cost of domestication? One can expect domestication to be involved with a substantial fitness cost, in the sense that domestic animals and plants would not do well in the wild. This cost can appear due to the following reasons: 1) Artificial selection for useless or even deleterious trait states (goldfish). 2) Artificial selection for useful trait states (a high yield of something) which, nevertheless, may reduce the overall fitness due to trade-offs. 3) Damaging side-effects of strong artificial selection, due to hitch-hiking of deleterious alleles. 4) Relaxation of negative selection protecting features that are important in the wild, but not in captivity. 5) Inbreeding. Genetic cost of domestication has recently been studied on dogs and rice.

25. Dogs have accumulated nonsynonymous substitutions in mitochondrial genes at a faster rate than wolves, leading to elevated levels of variation in their proteins, which indicates relaxed selective constraint. Relative rates of nonsynonymous substitutions. Values for wolves are indicated in blue, for dogs in yellow, and for the divergence between a random wolf and coyote sequence in red. A similar pattern has been observed in domesticated rice. Also, among non-synonymous substitutions fixed in the course of rice domestication, a fraction of radical substitutions, that involve two chemically dissimilar amino acids, is elevated.

26. Thus, wild progenitors and relatives of domesticated animals and plants remain a very valuable genetical resource. Although lacking some specific desirable qualities, produced by artificial selection, wild progenitors have healthier genotypes and may possess alleles which were lost in domesticated varieties. Wild (left) and domesticated cultivars (center, right) of sunflower. Like maize and potato, domestication of sunflower was a single event.

27. 2. Selection experiments Almost all attempts to select for something artificially were successful, in the sense that a substantial response to selection has been obtained. However, this response often diminishes with time - due to the population running out of genetic variation and/or to negative correlation between fitness and the trait states that are selected for. The numbers of abdominal and sternopleural bristles in Drosophila are two convenient and seemingly unimportant traits for artificial selection experiments.

28. Artificial selection for seemingly unimportant traits Replicated divergent artificial selection for abdominal and sternopleural bristle number from a highly inbred strain of Drosophila melanogaster resulted in an average divergence after 125 generations of selection of 12.0 abdominal and 8.2 sternopleural bristles from the accumulation of new mutations affecting bristle number. Decelerating responses to selection and rapid responses to reverse selection suggest new mutations affecting bristle number on average have deleterious effects on fitness.

29. Responses to 125 generations of selection for abdominal bristle number from an inbred base population. Closed symbols and solid lines give generation means of high bristle number replicates, and open symbols and dashed lines represent generation means of low bristle number replicates. Circles, triangles and squares indicate replicates 1, 2 and 3, respectively.

30. Responses to 125 generations of selection for sternopleural bristle number from an inbred base population. Closed symbols and solid lines give generation means of high bristle number replicates, and open symbols and dashed lines represent generation means of low bristle number replicates. Circles, triangles and squares indicate replicates 1, 2 and 3, respectively.

31. The Illinois Long-Term Selection Experiment This experiment on artificial selection for grain protein and oil concentration in maize (Zea mays) is the longest continuous genetics experiment in higher plants. The most striking observation is the significant degree of genetic variation remaining after more than 100 generations of selection. Selection response continues in all the populations except ILO and ILP, which have probably reached lower biological limits for these traits owing to their poor germination frequencies and lack of change in recent cycles. Further evidence for significant genetic variation is provided by the reverse selection experiments initiated at cycle 48.

32. Selection responses in the Illinois Protein Strains (a). Selection has been performed for 103 cycles in the Illinois High Protein (IHP) and Illinois Low Protein (ILP) strains. Selection was reversed in these strains beginning at cycle 48 to produce the Reverse High Protein (RHP) and Reverse Low Protein (RLP) strains.

33. Selection responses in the Illinois Oil Strains (b). Selection has been performed for 103 cycles in the Illinois High Oil (IHO) and Illinois Low Oil (ILO) strains. Selection was reversed in these strains beginning at cycle 48 to produce the Reverse High Oil (RHO) and Reverse Low Oil (RLO) strains.

34. Artificial selection for a certainly deleterious trait state It is possible to artificially select Drosophila melanogaster males for reduced sexual activity. In one such experiment, only those males who do not mate with any of the 4 virgin females in 30 minutes were allowed to reproduce (eventually). After several generations of such selection flies were in a rather bad shape - they hardly moved. Response to 280 generations of selection for low sexual activity. The ordinate shows the fraction of males that did not mate after 30 minutes.

35. 3. Evolution of captive populations In addition to experiments on active artificial selection, it is also possible to maintain a captive population, and to allow its individuals to perform selection on their own. Experimental evolution of Escherichia coli 1. Adaptation to a new environment. The dynamics of adaptation to a new environment of experimental populations of E. coli. Bacteria lived in a hemostat on a minimal medium with glucose as the only source of carbon. Fitness decelerated as the population approached a fitness peak.

36. 2. Decline of unused functions. The decline of catabolitic functions in the course of evolution with glucose as the only source of carbon, when these functions are not directly used. As expected, they declined, and this decline was faster in populations that acquired high mutation rate (dashed line) than in populations that kept low ancestral mutation rate (solid line).

37. 3. Homoplasy (parallelism) and unpredictability. Twelve initially identical populations of Escherichia coli evolved in identical environments for 20,000 cell generations. Mutations of unknown effect had been discovered in one population at four loci (pykF, nadR, pbpA-rodA, and hokB/sokB). Two of these genes, pykF and nadR, had substitutions in all 11 other populations, and the other two in several populations. There were only very few cases, however, in which the exact same mutations were fixed. Natural selection probably drove the parallel evolution of these four genes. Mutations fixed by 20,000 generations in 12 experimental populations of E. coli. Lighter regions indicate protein-coding sequences. Each arrow marks a mutation; the number shows the affected population.

38. 4. Cladogenesis and speciation. Two distinct types, designated L (large) and S (small) based on their colony morphology, arose by generation 6000 in an experimental population of Escherichia coli and coexisted for more than 12,000 generations thereafter. The derived S morph was monophyletic, indicating a long history of coexistence with L. Two factors enabled the stable coexistence of L and S. First, L excretes a metabolite that differentially promotes the growth of S. Second, L experiences increased death during the stationary phase (i. e., after glucose is depleted) when S is present. The relationship between the morphs was dynamic through time, with the frequency of S rising and falling several times between about 10–20% and 50–90% of the total population. Both lineages continued to adapt.

39. L and S individuals from different generations each form their own clade, demonstrating phylogenetic continuity of each lineage. Here, paleontological record is perfect, and is maintained in a freezer. Thus, we can reject the upper scenario. Instead, both L and S are two phylogenetically continuous lineages, derived once from a basal group.

40. Trajectories of genetic diversity within the S and L lineages. The data for L are shown as circles and solid lines; the data for S are shown as squares and dashed lines. Significant declines in genetic variation between consecutive samples are indicated by asterisks. Each lineage underwent periods of sharp decline in genetic variation, indicating selective sweeps due to fixations of beneficial mutations within the lineage. Thus, both L and S lineages continued to adapt following their origin. However, adaptation of one lineage did not cause extinction of the other lineage. Thus, S and L are distinct, sympatric populations.

41. Experimental evolution of a phage Bacteriophage fX174 evolved on a continuous supply of sensitive hosts for 180 days (~13,000 phage generations). The average rate of nucleotide substitution was ~0.2% (11 substitutions)/20 days, and substitutions accumulated in a clock-like manner throughout the study. Most of the changes were adaptive, even many of the silent substitutions. The sustained, high rate of adaptive evolution defies a model of adaptation to a constant environment. Perhaps, continuing molecular evolution reflects a potentially indefinite arms race, stemming from high levels of co-infection and the resulting conflict among genotypes competing within the same cell. Changes in the fX174 hemostat population. Solid diamonds show the number of differences between each sequenced isolate and the ancestral sequence. Open triangles show the distance between pairs of isolates from the same time point.

42. 4. Rapid evolution in the wild Rapid evolution is often triggered by rapid changes of the environment. The most salient cases are due to changes induced by humans, although rapid evolution in the wild due to natural causes has also been observed. Peppered moth Biston betularia Two extreme morphs of Biston betularia, typica (light) and carbonaria (dark).

43. In peppered moth, the ancestral phenotype is light-gray (morph typica), which provides some protection against birds on tree trunks that are covered by lichens. In the XIX century, pollution due to coal burning killed lichens over much of England, and morph carbonaria became common in the affected areas. At mid-20th century a steep cline of carbonaria frequency running from the north of Wales to the southern coast of England separated a region of <5% to west from >90% to northeast. At that time pollution was greatly reduced. By the 1980s the plateau of 90% frequency of carbonaria had contracted to northern England. The frequency has since continued to drop so that the maximum is now less than 50% and in most places below 10%. The observed changes require 5%-20% selection against carbonaria.The advantage of carbonaria was large in areas of heavy pollution where typica frequencies were 20% or less. carbonaria frequencies at three successive times: (a) Mid-20th century; (b)1983-1984; (c) 1987-1999.

44. Rapid evolution of plants Mining and industry create high local levels of soil pollution with zinc, copper, and lead. A wide variety of plant species rapidly adapt to this pollution. Arabidopsis halleri, a species that now contains a number of metallophyte (M) populations that can grow in the presence of heavy metals, as well as ancestral NM populations that cannot. Geographically isolated M populations are more closely related to their closest NM populations than to each other. This is one more example of homoplasy.

45. Geographic distribution of Arabidopsis halleri genotypes. Metallophyte populations are shown in red, nonmetallophyte ones in blue.

46. Multiple origin of metallophyte Arabidopsis halleri (Brassicaceae) in central Europe. Populations of Arabidopsis halleri that are geographically close to each other are also tightly related. Thus, the ability to tolerate zinc evolved many times independently.

47. 5. Rapid evolution of human pathogens Both emergence of new pathogens and evolution of existing pathogens are very important. Emergence of new pathogens A relatively new human pathogen Mycobacterium leprae is undergoing a massive pseudogenesation. From the outside: circles 1 and 2 (clockwise and anticlockwise) genes on the - and + strands, respectively; circles 3 and 4, pseudogenes; 5 and 6, M. leprae specific genes; 7, repeat sequences; 8, G+C content; 9, G/C bias (G+C)/(G-C).

48. Emergence of an infectious disease. New pathogens emerge from animal reservoirs. Effective human-to-human transmission requires that the pathogen's basic reproductive number, R0, should exceed one, where R0 is the average number of secondary infections arising from one infected individual in a completely susceptible population. Introductions from the reservoir are followed by chains of transmission in the human population. Infections with the introduced strain (open circles) have R0 < 1. Pathogen evolution generates an evolved strain (filled circles) with R0 > 1. The infections caused by the evolved strain can go on to cause an epidemic. Daggers indicate no further transmission.

49. Evolution of SARS coronavirus Coronavirus that causes severe acute respiratory syndrome (SARS) in humans is a pathogen of palm civets. Phylogenetic analysis suggests that there were two independent transmissions of the virus to humans, one that caused 2002-2003 epidemic and the other that caused 2003-2004 outbreak in the city of Guangzhou. The virus evolves very rapidly within both hosts, and the ratio of nonsynonymous/synonymous nucleotide substitution is very high, suggesting rapid adaptation. Major genetic variations in some critical genes, particularly the Spike gene, are essential for the transition from animal-to-human transmission to human-to-human transmission. PC prefix is for viruses isolated from palm civet and HP for viruses isolated from human patients. Both of them were suffixed with 03 or 04 to specify the 2002–2003 or 2003–2004 epidemics, respectively.

50. Detailed phylogeny of SARS-CoV covering the epidemics from 2002 to 2004.