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Laboratory experiments of speciation

Topic: Organization

 From HandWiki - Reading time: 13 min
Short description: Biological experiments
A simplification of an allopatric speciation experiment where two lines of fruit flies are raised on maltose and starch media

Laboratory experiments of speciation have been conducted for all four modes of speciation: allopatric, peripatric, parapatric, and sympatric; and various other processes involving speciation: hybridization, reinforcement, founder effects, among others. Most of the experiments have been done on flies, in particular Drosophila fruit flies.[1] However, more recent studies have tested yeasts, fungi, and even viruses.

It has been suggested that laboratory experiments are not conducive to vicariant speciation events (allopatric and peripatric) due to their small population sizes and limited generations.[2] Most estimates from studies of nature indicate that speciation takes hundreds of thousands to millions of years.[3] On the other hand, many species are thought to have speciated faster and more recently, such as the European flounders (Platichthys flesus) that spawn in pelagic and demersal zones—having allopatrically speciated in under 3000 generations.[4]

Table of experiments

Six publications have attempted to compile, review, and analyze the experimental research on speciation:

  1. John Ringo, David Wood, Robert Rockwell, and Harold Dowse in 1985;[5]
  2. William R. Rice and Ellen E. Hostert in 1993;[6]
  3. Ann-Britt Florin and Anders Ödeen in 2002;[2]
  4. Mark Kirkpatrick and Virginie Ravigné in 2002;[7]
  5. Jerry A. Coyne and H. Allen Orr in 2004;[1] and
  6. James D. Fry in 2009.[8]

The table summarizes the studies and data reviewed in these publications. It also references several contemporary experiments and is non-exhaustive. In the table, multiple numbers separated by semi-colons in the generations column indicate that multiple experiments were conducted. The replications (in parentheses) indicates the number of populations used in the experiments—i.e. how many times the experiment was replicated. Various types of selection have been imposed on experimental populations and are indicated by the selection type column. Negative or positive results of each experiment are provided by the reproductive isolation column. Pre-zygotic reproductive isolation means that the reproducing individuals in the populations were unable to produce offspring (effectively a positive result). Post-zygotic isolation means that the reproducing individuals were able to produce offspring but they were either sterile or inviable (a positive result as well). Negative results are indicated by "none"—that is, the experiments did not result in reproductive isolation.

Laboratory experiments of speciation[1][6][7][2][8]
Species Trait Generations (replications) [duration] Tested Selection type Studied genetic drift Reproductive isolation Reference Year
Drosophila melanogaster Escape response 18 Vicariant, reinforcement, parapatric/

sympatric

Indirect; divergent Yes Pre-zygotic Grant & Mettler[9] 1969
D. melanogaster Locomotion 112 Vicariant Indirect; divergent No Pre-zygotic Burnet & Connolly[10] 1974
D. melanogaster Temperature, humidity 70–130 Vicariant Indirect; divergent Yes Pre-zygotic Kilias et al.[11] 1980
D. melanogaster DDT adaptation 600 [25 years, +15 years] Vicariant Direct No Pre-zygotic Boake et al.[12] 2003
D. melanogaster 17, 9, 9, 1, 1, 7, 7, 7, 7 Vicariant; parapatric/

sympatric

Direct, divergent Pre-zygotic in vicariance; none with gene flow Barker & Karlsson[13] 1974
D. melanogaster 40; 50 Reinforcement Direct; divergent Pre-zygotic Crossley[14] 1974
D. melanogaster Locomotion 45 Vicariant Direct; divergent No None van Dijken & Scharloo[15][16] 1979
D. melanogaster Reinforcement Direct; divergent Pre-zygotic Wallace[17] 1953
D. melanogaster 36; 31 Reinforcement Direct; divergent Pre-zygotic Knight[18] 1956
D. melanogaster EDTA adaptation 25, 25, 25, 14 Semi-allopatric, reinforcement Indirect; divergent No Post-zygotic Robertson[19][20] 1966
D. melanogaster 25 (8) Vicariant; reinforcement; parapatric; sympatric Direct None Hostert[21] 1997
D. melanogaster Abdominal chaeta

number

21–31 Vicariant Direct Yes None Santibanez & Waddington[22] 1958
D. melanogaster Sternopleural chaeta number 32 Vicariant, reinforcement, parapatric/

sympatric

Direct No None Barker & Cummins[23] 1969
D. melanogaster Phototaxis, geotaxis 20 Vicariant No None Markow[24][25] 1975; 1981
D. melanogaster Peripatric Yes Rundle et al.[26] 1998
D. melanogaster Vicariant; peripatric Yes Mooers et al.[27] 1999
D. melanogaster 12 Reinforcement Divergent Pre-zygotic Thoday & Gibson[28] 1962
D. melanogaster None Thoday & Gibson[29][30] 1970; 1971
D. melanogaster 16 Reinforcement Indirect None Spiess & Wilke[31] 1954
D. melanogaster Reinforcement Direct; divergent Pre-zygotic Ehrman[32][33][34][35] 1971; 1973; 1979; 1983
D. melanogaster Sternopleural chaeta number 5; 27; 27; 1; 1; 1; 1; 1 Parapatric/

sympatric

None Chabora[36] 1968
D. melanogaster None Scharloo[37] 1967
D. melanogaster 1, 1 Coyne & Grant[38] 1972
D. melanogaster 25 Rice[39] 1985
D. melanogaster 25 Disruptive Pre-zygotic Rice & Salt[40] 1988
D. melanogaster 35; 35 Sympatric Pre-zygotic Rice & Salt[41] 1990
D. melanogaster NaCl and CuSO4 levels in food [3 years in allopatry, 1 in sympatry] Allopatric; reinforcement; sympatric Pre-zygotic in allopatry, none in sympatry Wallace[42] 1982
D. melanogaster Reinforcement Ehrman et al.[43] 1991
D. melanogaster Reinforcement Fukatami & Moriwaki[44] 1970
Drosophila simulans Scutellar bristles, development speed, wing width; desiccation resistance, fecundity, ethanol resistance; courtship display, re-mating speed, lek behavior; pupation height, clumped egg laying, general activity [3 years] Vicariant; peripatric Yes Post-zygotic Ringo et al.[5] 1985
Drosophila paulistorum 131; 131 Reinforcement Direct Pre-zygotic Dobzhansky et al.[45] 1976
D. paulistorum [5 years] Vicariant Dobzhansky and Pavlovsky[46] 1966
Drosophila willistoni pH adaptation 34–122 Vicariant Indirect; divergent No Pre-zygotic Kalisz & Cordeiro[47] 1980
Drosophila pseudoobscura Carbohydrate source 12 Vicariant Indirect Yes Pre-zygotic Dodd[48] 1989
D. pseudoobscura Temperature adaptation 25–60 Vicariant Direct Ehrman[49][50][51][52][53] 1964;

1969

D. pseudoobscura Phototaxis, geotaxis 5–11 Vicariant Indirect No Pre-zygotic del Solar[54] 1966
D. pseudoobscura Vicariant; peripatric Pre-zygotic Powell[55][56] 1978; 1985
D. pseudoobscura Peripatric; vicariant Yes Galiana et al.[57] 1993
D. pseudoobscura Temperature photoperiod; food 37 (78) [33–34 months] Vicariant Divergent Yes None Rundle[58] 2003
D. pseudoobscura &

Drosophila persimilis

22; 16; 9 Reinforcement Direct; divergent Pre-zygotic Koopman[59] 1950
D. pseudoobscura &

D. persimilis

18 (4) Direct Pre-zygotic Kessler[60] 1966
Drosophila mojavensis 12 Direct Pre-zygotic Koepfer[61] 1987
D. mojavensis Development time 13 Divergent Yes None Etges[62] 1998
Drosophila adiastola Peripatric Yes Pre-zygotic Arita & Kaneshiro[63] 1974
Drosophila silvestris Peripatric Yes Ahearn[64] 1980
Musca domestica Geotaxis 38 Vicariant Indirect No Pre-zygotic Soans et al.[65] 1974
M. domestica Geotaxis 16 Vicariant Direct; divergent No Pre-zygotic Hurd & Eisenburg[66] 1975
M. domestica Peripatric Yes Meffert & Bryant[67] 1991
M. domestica Regan et al.[68] 2003
Bactrocera cucurbitae Development time 40–51 Divergent Yes Pre-zygotic Miyatake & Shimizu[69] 1999
Zea mays 6; 6 Reinforcement Direct; divergent Pre-zygotic Paterniani[70] 1969
Drosophila grimshawi Peripatric Jones, Widemo, & Arrendal[71] N/A
Saccharomyces cerevisiae Leu & Murry[72] 2006
D. melanogaster Reinforcement Harper & Lambert[73] 1983
Tribolium castaneum Pupal weight 15 (6) Disruptive Halliburton & Gall[74] 1983
D. melanogaster Geotaxis Divergent Lofdahl et al.[75] 1992
D. pseudoobscura [10 years] Moya et al.[76] 1995
Neurospora Divergent Dettman et al.[77] 2008
S. cerevisiae 500 Divergent Dettman et al.[78] 2007
Sepsis cynipsea 35 Martin & Hosken[79] 2003
D. melanogaster Wigby & Chapman[80] 2006
D. pseudoobscura Sexual conflict 48–52 (4; 4; 4) Bacigalupe et al.[81] 2007
D. serrata Rundle et al.[82] 2005
Drosophila serrata & D. birchii Mate recognition 9 (3; 3) Reinforcement Natural Pre-zygotic Higgie et al.[83] 2000
Enterobacteria phage λ Escherichia coli receptor exploitation 35 cycles (6) Vicariant, sympatric Pre-zygotic Meyer et al.[84] 2016
Tetranychus urticae Resistance to host plant toxin Overmeer[85] 1966
T. urticae Resistance to host plant toxin Fry[86] 1999
Helianthus annus × H. petiolaris and H. anomalus Hybrid Rieseburg et al.[87] 1996
S. cerevisiae 2002
D. melanogaster Life history Ghosh & Joshi[88] 2012
Drosophila subobscura Mate behavior Bárbaro et al.[89] 2015
Digital organisms ~42,000; ~850 (20) Ecological Post-zygotic Anderson & Harmon[90] 2014
Schizosaccharomyces pombe Complete reproductive isolation Seike et al.[91] 2015
D. pseudoobscura Courtship song 130 Debelle et al.[92] 2014
Callosobruchus maculatus 40 (16) Debelle et al.[93] 2010

See also

References

  1. ↑ 1.0 1.1 1.2 Coyne, Jerry A.; Orr, H. Allen (2004), Speciation, Sinauer Associates, pp. 1–545, ISBN 978-0-87893-091-3 
  2. ↑ 2.0 2.1 2.2 Florin, Ann-Britt & Ödeen, Anders (2002), "Laboratory environments are not conducive for allopatric speciation", Journal of Evolutionary Biology 15 (1): 10–19, doi:10.1046/j.1420-9101.2002.00356.x 
  3. ↑ Coyne, Jerry A.; Orr, H. Allen (1997), ""Patterns of Speciation in Drosophila" Revisited", Evolution 51 (1): 295–303, doi:10.1111/j.1558-5646.1997.tb02412.x, PMID 28568795 
  4. ↑ Momigliano, Paolo; Jokinen, Henri; Fraimout, Antoine; Florin, Ann-Britt; Norkko, Alf; Merilä, Juha (2017), "Extraordinarily rapid speciation in a marine fish", PNAS 114 (23): 6074–6079, doi:10.1073/pnas.1615109114, PMID 28533412, PMC 5468626, Bibcode: 2017PNAS..114.6074M, http://www.pnas.org/content/pnas/114/23/6074.full.pdf 
  5. ↑ 5.0 5.1 Ringo, John; Wood, David; Rockwell, Robert; Dowse, Harold (1985), "An Experiment Testing Two Hypotheses of Speciation", The American Naturalist 126 (5): 642–661, doi:10.1086/284445 
  6. ↑ 6.0 6.1 Rice, William R. & Hostert, Ellen E. (1993), "Laboratory Experiments on Speciation: What Have We Learned in 40 Years?", Evolution 47 (6): 1637–1653, doi:10.1111/j.1558-5646.1993.tb01257.x, PMID 28568007 
  7. ↑ 7.0 7.1 Kirkpatrick, Mark & Ravigné, Virginie (2002), "Speciation by Natural and Sexual Selection: Models and Experiments", The American Naturalist 159: S22–S35, doi:10.1086/338370, PMID 18707367 
  8. ↑ 8.0 8.1 Fry, James D. (2009). Laboratory Experiments on Speciation. In Garland, Theodore & Rose, Michael R. "Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments". Pp. 631–656. doi:10.1525/california/9780520247666.003.0020
  9. ↑ Grant, B. S. & Mettler, L. E. (1969), "Disruptive and stabilizing selection on the" escape" behavior of Drosophila melanogaster", Genetics 62 (3): 625–637, doi:10.1093/genetics/62.3.625, PMID 17248452 
  10. ↑ Burnet, B. & Connolly, K. (1974). Activity and sexual behavior in Drosophila melanogaster. In Abeelen, J. H. V. F. (eds). The Genetics of Behaviour. North-Holland, Amsterdam. Pp. 201–258.
  11. ↑ Kilias, G., Alahiotis, S. N., & Pelecanos, M. (1980), "A Multifactorial Genetic Investigation of Speciation Theory Using Drosophila melanogaster", Evolution 34 (4): 730–737, doi:10.2307/2408027, PMID 28563991 
  12. ↑ Boake, C. R. B., Mcdonald, K., Maitra, S., Ganguly, R. (2003), "Forty years of solitude: life-history divergence and behavioural isolation between laboratory lines of Drosophila melanogaster", Journal of Evolutionary Biology 16 (1): 83–90, doi:10.1046/j.1420-9101.2003.00505.x, PMID 14635883 
  13. ↑ Barker, J. S. F. & Karlsson, L. J. E. (1974), "Effects of population size and selection intensity on responses to disruptive selection in Drosophila melanogaster", Genetics 78 (2): 715–735, doi:10.2307/2407287, PMID 4217303 
  14. ↑ Crossley, Stella A. (1974), "Changes in Mating Behavior Produced by Selection for Ethological Isolation Between Ebony and Vestigial Mutants of Drosophila melanogaster", Evolution 28 (4): 631–647, doi:10.1111/j.1558-5646.1974.tb00795.x, PMID 28564833 
  15. ↑ van Dijken, F. R. & Scharloo, W. (1979), "Divergent selection on locomotor activity in Drosophila melanogaster. I. Selection response", Behavior Genetics 9 (6): 543–553, doi:10.1007/BF01067350, PMID 122270 
  16. ↑ van Dijken, F. R. & Scharloo, W. (1979), "Divergent selection on locomotor activity in Drosophila melanogaster. II. Test for reproductive isolation between selected lines", Behavior Genetics 9 (6): 555–561, doi:10.1007/BF01067351, PMID 122271 
  17. ↑ Wallace, B. (1953), "Genetic divergence of isolated populations of Drosophila melanogaster", Proceedings of the Ninth International Congress of Genetics 9: 761–764 
  18. ↑ Knight, G. R., Robertson, Alan, & Waddington, C. H. (1956), "Selection for sexual isolation within a species", Evolution 10 (1): 14–22, doi:10.1111/j.1558-5646.1956.tb02825.x 
  19. ↑ Robertson, Forbes W. (1966), "A test of sexual isolation in Drosophila", Genetical Research 8 (2): 181–187, doi:10.1017/S001667230001003X, PMID 5922518 
  20. ↑ Robertson, Forbes W. (1966), "The ecological genetics of growth in Drosophila 8. Adaptation to a New Diet", Genetical Research 8 (2): 165–179, doi:10.1017/S0016672300010028, PMID 5922517 
  21. ↑ Hostert, Ellen E. (1997), "Reinforcement: a new perspective on an old controversy", Evolution 51 (3): 697–702, doi:10.1111/j.1558-5646.1997.tb03653.x, PMID 28568598 
  22. ↑ Koref Santibañez, S. & Waddington, C. H. (1958), "The origin of sexual isolation between different lines within a species", Evolution 12 (4): 485–493, doi:10.2307/2405959 
  23. ↑ Barker, J. S. F. & Cummins, L. J. (1969), "The effect of selection for sternopleural bristle number in mating behaviour in Drosophila melanogaster", Genetics 61 (3): 713–719, doi:10.1093/genetics/61.3.713, PMID 17248436 
  24. ↑ Markow, Therese Ann (1975), "A genetic analysis of phototactic behavior in Drosophila melanogaster", Genetics 79 (3): 527–534, doi:10.1093/genetics/79.3.527, PMID 805084 
  25. ↑ Markow, Therese Ann (1981), "Mating preferences are not predictive of the direction of evolution in experimental populations of Drosophila", Science 213 (4514): 1405–1407, doi:10.1126/science.213.4514.1405, PMID 17732575, Bibcode: 1981Sci...213.1405M 
  26. ↑ Rundle, H. D., Mooers, Arne Ø. & Whitlock, Michael C. (1998), "Single founder-flush events and the evolution of reproductive isolation", Evolution 52 (6): 1850–1855, doi:10.1111/j.1558-5646.1998.tb02263.x, PMID 28565304 
  27. ↑ Mooers, Arne Ø., Rundle, Howard D. & Whitlock, Michael C. (1999), "The effects of selection and bottlenecks on male mating success in peripheral isolates", American Naturalist 153 (4): 437–444, doi:10.1086/303186, PMID 29586617 
  28. ↑ Thoday, J. M. & Gibson, J. B. (1962), "Isolation by disruptive selection", Nature 193 (4821): 1164–1166, doi:10.1038/1931164a0, PMID 13920720, Bibcode: 1962Natur.193.1164T 
  29. ↑ Thoday, J. M. & Gibson, J. B. (1970), "The probability of isolation by disruptive selection", Nature 104 (937): 219–230, doi:10.1086/282656 
  30. ↑ Scharloo, W. (1971), "Reproductive isolation by disruptive selection: Did it occur?", American Naturalist 105 (941): 83–86, doi:10.1086/282706 
  31. ↑ Spiess, E. B. & Wilke, C. M. (1984), "Still another attempt to achieve assortive mating by disruptive selection in Drosophila", Evolution 38 (3): 505–515, doi:10.2307/2408700, PMID 28555983 
  32. ↑ Ehrman, Lee (1971), "Natural selection and the origin of reproductive isolation", American Naturalist 105 (945): 479–483, doi:10.1086/282739 
  33. ↑ Ehrman, Lee (1973), "More on natural selection and the origin of reproductive isolation", American Naturalist 107 (954): 318–319, doi:10.1086/282835 
  34. ↑ Ehrman, Lee (1979), "Still more on natural selection and the origin of reproductive isolation", American Naturalist 113 (1): 148–150, doi:10.1086/283371 
  35. ↑ Ehrman, Lee (1983), "Fourth report on natural selection for the origin of reproductive isolation", American Naturalist 121 (2): 290–293, doi:10.1086/284059 
  36. ↑ Chabora, Alice J. (1968), "Disruptive selection for sternopleural chaeta number in various strains of Drosophila melanogaster", American Naturalist 102 (928): 525–532, doi:10.1086/282565 
  37. ↑ Scharloo, W., Hoogmoed, M. S. & Kuile, A. T. (1967), "Stabilizing and disruptive selection on a mutant character in Drosophila. I. The phenotypic variance and its components.", Genetics 56 (4): 709–726, doi:10.1093/genetics/56.4.709, PMID 6061662 
  38. ↑ Coyne, Jerry A. & and Grant, Bruce (1972), "Disruptive selection on I-maze activity in Drosophila melanogaster", Genetics 71 (1): 185–188, doi:10.1093/genetics/71.1.185, PMID 17248572 
  39. ↑ Rice, W. R. (1985), "Disruptive selection on habitat preference and the evolution of reproductive isolation: an exploratory experiment", Evolution 39 (3): 645–656, doi:10.1111/j.1558-5646.1985.tb00401.x, PMID 28561974 
  40. ↑ Rice, William R. & Salt, George, W. (1988), "Speciation via disruptive selection on habitat preference", American Naturalist 131 (6): 911–917, doi:10.1086/284831 
  41. ↑ Rice, William R. & Salt, George, W. (1990), "The evolution of reproductive isolation as a correlated character under sympatric conditions: experimental evidence", Evolution 44 (5): 1140–1152, doi:10.2307/2409278, PMID 28563894 
  42. ↑ Wallace, B. (1982), "Drosophila melanogaster populations selected for resistances to NaCl and CuSO4 in both allopatry and sympatry", Journal of Heredity 73 (1): 35–42, doi:10.1093/oxfordjournals.jhered.a109572, PMID 6802898 
  43. ↑ Ehrman, Lee, White, Marney A. & Wallace, B. (1991). A long-term study involving Drosophila melanogaster and toxic media. In Hecht, M. K., Wallace, B., & Maclntyre, R. J. (eds). Evolutionary biology, vol. 25. Plenum Press, New York. Pp. 175–209
  44. ↑ Fukatami, A & Moriwaki, D. (1970), "Selection for sexual isolation in Drosophila melanogaster by a modification of Koopman's method", The Japanese Journal of Genetics 45 (3): 193–204, doi:10.1266/jjg.45.193 
  45. ↑ Dobzhansky, Theodosius; Pavlovsky, O.; Powell, J. R. (1976), "Partially Successful Attempt to Enhance Reproductive Isolation Between Semispecies of Drosophila paulistorum", Evolution 30 (2): 201–212, doi:10.2307/2407696, PMID 28563045 
  46. ↑ Dobzhansky, Theodosius & Pavlovsky, O. (1966), "Spontaneous origin of an incipient species in the Drosophila paulistorum complex", Proceedings of the National Academy of Sciences 55 (4): 723–733, doi:10.1073/pnas.55.4.727, PMID 5219677, Bibcode: 1966PNAS...55..727D 
  47. ↑ de Oliveira, Alice Kalisz & Cordeiro, Antonio Rodrigues (1980), "Adaptation of Drosophila willistoni experimental populations to extreme pH medium", Heredity 44: 123–130, doi:10.1038/hdy.1980.11 
  48. ↑ Dodd, Diane M. B. (1989), "Reproductive Isolation as a Consequence of Adaptive Divergence in Drosophila pseudoobscura", Evolution 43 (6): 1308–1311, doi:10.2307/2409365, PMID 28564510 
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  54. ↑ del Solar, Eduardo (1966), "Sexual isolation caused by selection for positive and negative phototaxis and geotaxis in Drosophila pseudoobscura", Proceedings of the National Academy of Sciences 56 (2): 484–487, doi:10.1073/pnas.56.2.484, PMID 5229969 
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  59. ↑ Koopman, Karl F. (1950), "Natural Selection for Reproductive Isolation Between Drosophila pseudoobscura and Drosophila persimilis", Evolution 4 (2): 135–148, doi:10.2307/2405390 
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  63. ↑ Arita, Lorna H. & Kaneshiro, Kenneth Y. (1979), "Ethological Isolation Between Two Stocks of Drosophila Adiastola Hardy", Hawaiian Entomological Society 23 (1): 31–34 
  64. ↑ Ahearn, J. N. (1980), "Evolution of behavioral reproductive isolation in a laboratory stock of Drosophila silvestris", Experientia 36 (1): 63–64, doi:10.1007/BF02003975 
  65. ↑ Soans, A. Benedict; Pimentel, David; Soans, Joyce S. (1974), "Evolution of Reproductive Isolation in Allopatric and Sympatric Populations", The American Naturalist 108 (959): 117–124, doi:10.1086/282889 
  66. ↑ Hurd, L. E. & Eisenberg, Robert M. (1975), "Divergent Selection for Geotactic Response and Evolution of Reproductive Isolation in Sympatric and Allopatric Populations of Houseflies", The American Naturalist 109 (967): 353–358, doi:10.1086/283002 
  67. ↑ Meffert, L. M. & Bryant, E. H. (1991), "Mating propensity and courtship behavior in serially bottlenecked lines of the housefly", Evolution 45 (2): 293–306, doi:10.1111/j.1558-5646.1991.tb04404.x, PMID 28567864 
  68. ↑ Regan, J. L.; Meffert, L. M.; Bryant, E. H. (2003), "A direct experimental test of founder-flush effects on the evolutionary potential for assortative mating", Journal of Evolutionary Biology 16 (2): 302–312, doi:10.1046/j.1420-9101.2003.00521.x, PMID 14635869 
  69. ↑ Miyatake, Takahisa & Shimizu, Toru (1999), "Genetic correlations between life-history and behavioral traits can cause reproductive isolation", Evolution 53 (1): 201–208, doi:10.2307/2640932, PMID 28565193 
  70. ↑ Paterniani, E. (1969), "Selection for Reproductive Isolation between Two Populations of Maize, Zea mays L.", Evolution 23 (4): 534–547, doi:10.2307/2406851, PMID 28562870 
  71. ↑ Ödeen, Anders & Florin, Ann-Britt (2002), "Sexual selection and peripatric speciation: the Kaneshiro model revisited", Journal of Evolutionary Biology 15 (2): 301–306, doi:10.1046/j.1420-9101.2002.00378.x 
  72. ↑ Leu, J. Y. & Murray, A. W. (2006), "Experimental evolution of mating discrimination in budding yeast", Current Biology 16 (3): 280–286, doi:10.1016/j.cub.2005.12.028, PMID 16461281 
  73. ↑ Harper, A. A. & Lambert, D. M. (1983), "The population genetics of reinforcing selection", Genetica 62 (1): 15–23, doi:10.1007/BF00123305 
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