The gap between evolutionary studies in laboratory versus natural populations is a persistent problem

Harshman, Lawrence G.

Hoffmann, Ary A.

Levy, André

Matos, Margarida

Rose, Michael R.

Teotónio, Henrique

English

DigitalCommons@University of Nebraska

University of Nebraska - LincolnDigitalCommons@University of Nebraska - LincolnLawrence G. Harshman Publications Papers in the Biological Sciences5-2000"An Evolutionary No Man’s Land" and "Reply fromL. G. Harshman and A. A. Hoffmann"Margarida MatosFaculdade de Ciências de Lisboa, mmatos@fc.ul.ptAndré LevyState University of New York, Stony Brook, andrec@life.bio.sunysb.eduHenrique TeotónioUniversity of California, Irvine, teotonio@uci.eduMichael R. RoseUniversity of California, Irvine, mmrose@uci.eduLawrence G. HarshmanUniversity of Nebraska–Lincoln, lharshman1@unl.eduSee next page for additional authorsFollow this and additional works at: http://digitalcommons.unl.edu/biosciharshmanPart of the Entomology Commons, and the Genetics CommonsThis Letter to the Editor is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University ofNebraska - Lincoln. It has been accepted for inclusion in Lawrence G. Harshman Publications by an authorized administrator ofDigitalCommons@University of Nebraska - Lincoln.Matos, Margarida; Levy, André; Teotónio, Henrique; Rose, Michael R.; Harshman, Lawrence G.; and Hoffmann, Ary A., ""AnEvolutionary No Man’s Land" and "Reply from L. G. Harshman and A. A. Hoffmann"" (2000). Lawrence G. Harshman Publications. 28.http://digitalcommons.unl.edu/biosciharshman/28AuthorsMargarida Matos, André Levy, Henrique Teotónio, Michael R. Rose, Lawrence G. Harshman, and Ary A.HoffmannThis letter to the editor is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/biosciharshman/28   Published in Correspondence, Trends in Ecology and Evolution 15:5 (May 2000), pp. 206, 207. Copyright © 2000 Elsevier Science Ltd. Used by permission. An Evolutionary No Man’s Land The gap between evolutionary studies in laboratory versus natural populations is a persis-tent problem.1,2 In an attempt to bridge this gap, some researchers in the early 1980s stud-ied the quantitative genetics of laboratory populations recently founded from the wild, with and without inbreeding.3,4 The dangers of such approaches were soon demonstrated experimentally.5,6 Inbreeding depression and genotype-by-environment interactions make such studies unreliable guides to the evolution of populations long-established in any en-vironment. This conclusion is reiterated to some extent in Harshman and Hoffmann’s re-cent TREE perspective,2 where the authors state that “The nature of laboratory selection regimes is unnatural.” But, they then go on to propose complementing selection experi-ments in long-established laboratory populations with selection experiments in recently introduced ones. It is not clear how one could disentangle the causes of possible differences from the results of such disparate studies. Furthermore, from first principles and extant experimental studies, we expect a conflation of evolutionary effects in the recently intro-duced populations because of adaptation to the laboratory environment, and because of genetic and evolutionary disequilibrium. In particular, interactions between adaptation to the general laboratory environment and any particular selective regime under study could be a source of unresolvable evolutionary outcomes, as we will now explain. Two evolutionary processes are at work in the transition from the wild to the laboratory. First, placing a population in a novel environment can cause a change in genetic variances and covariances between traits, as a result of genotype-by-environment interactions. Sec-ond, continued maintenance in this novel environment might bring about evolutionary change, perhaps because of new selection pressures or changes in breeding structure. A recently founded laboratory population will thus be in a “no man’s land.” We cannot use it to provide information about the original wild population, nor can we test evolutionary models that rely on the assumption that the newly transplanted population is near genetic or selective equilibrium. Surprisingly, like Harshman and Hoffmann, several recent stud-ies have essentially repeated these mistakes.7–9 Let us conclude with an example. The empirical challenge posed by the transition from wild to laboratory conditions led us to study the evolution of a newly founded laboratory population of Drosophila subobscura.10 We found that adaptation to the novel, laboratory environment occurred at a relatively fast rate. As an illustration, fecundity around the age of reproduction increased steadily in the generations after establishment in the laboratory, showing convergence to the values of a long-established population serving as a control C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  2 (maintained in the lab for 24 generations before the foundation of the new one); the fecun-dity of the new population became similar to that of the long-established population after just 14 generations of adaptation to the laboratory. In this no man’s land between the wild and the laboratory, the population evolved extremely rapidly. Instead of straining for du-bious interpretations of the uncertain results afforded by studies of recently sampled pop-ulations, we might use the gap between the wild and the laboratory as an evolutionary tool—recognizing that, after all, the lab is just another environment to which populations adapt, albeit a very peculiar one.10 To this extent, we can agree with Harshman and Hoff-mann.  Margarida Matos Carla Rego Centro de Biologia Ambiental, Departamento de Zoologia e Antropologia, Faculdade de Ciências de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal (mmatos@fc.ul.pt; crego@fc.ul.pt)  André Levy Department of Ecology and Evolution, State University of New York, Stony Brook, NY 11794-5245, USA (andrec@life.bio.sunysb.edu)  Henrique Teotónio Michael R. Rose Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525, USA (teotonio@uci.edu; mrrose@uci.edu)  References  1. Rose, M. R., and Lauder, G. V., eds. (1996) Adaptation, Academic Press. 2. Harshman, L. G., and Hoffmann, A. A. (2000) Laboratory selection experiments using Drosophila: what do they really tell us? Trends Ecol. Evol. 15, 32–36. 3. Dingle, H., and Hegmann, J.,P., eds. (1982) Evolution and Genetics of Life Histories, Springer-Verlag. 4. Giesel, J. T. (1986) Genetic correlation structure of life history variables in outbred, wild Drosoph-ila melanogaster : effects of photoperiod regimen. Am. Nat. 128, 593–603. 5. Rose, M. R. (1984) Genetic covariation in Drosophila life history: untangling the data. Am. Nat. 123, 565–569. 6. Service, P. M., and Rose, M. R. (1985) Genetic covariation among life-history components: the effect of novel environments. Evolution 39, 943–945. 7. Blanckenhorn, W. U., et al. (1998) Fluctuating asymmetry, body size, and sexual selection in the dung fly Sepsis cynipsea—testing the good genes assumptions and predictions. J. Evol. Biol. 11, 735–753. 8. Reusch, T., and Blanckenhorn, W. U. (1998) Quantitative genetics of the dung fly Sepsis cynipsea: Cheverud’s conjecture revisited. Heredity 81, 111–119. 9. Windig, J. J. (1999) Trade-offs between melanization, development time, and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity 82, 57–68. 10. Matos, M., et al. (2000) Adaptation to the laboratory environment in Drosophila subobscura. J. Evol. Biol. 13, 9–19. C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  3 Reply from L. G. Harshman and A. A. Hoffmann It has been argued that laboratory evolution experiments are superior to comparative stud-ies1,2 and phenotypic manipulations3 for the study of evolution. It has also been argued that there are constraints on the design of most field evolution studies compared with la-boratory evolution experiments,3 and suggested that interpreting the results of field evo-lutionary studies is problematical relative to laboratory evolution experiments.3 However, a crucial perspective on laboratory evolution studies calls these points of view into ques-tion. As we discussed in our recent TREE article,4 there is a range of problems associated with laboratory selection experiments using Drosophila to study the evolution of life history and stress-related traits. In their letter, Matos et al.5 did not significantly address any of the issues we raised.4 Their reply5 is a bit puzzling because their argument is similar to the one we presented.4 Like us, they describe the problem associated with conducting selection experiments using populations recently established in the laboratory. Specifically, we stated that “There is some evidence that Drosophila can adapt rapidly to laboratory culture,6 reducing the con-cern about using populations maintained in the laboratory for only a short term. Never-theless, it is unclear how many generations are required to dampen any spurious correlations potentially generated by domestication. To illuminate this issue, it is im-portant to investigate the process of Drosophila domestication in terms of the time course of changes in life history and of stress-related traits, and to investigate the patterns of ge-netic correlations among traits.”7 Once we have such information, it can be used as a basis to decide how long to maintain populations in the laboratory before initiating selection experiments; recommendations can be made about any likely confounding effects; and general guidelines could be established for comparing recently established and long-established populations. In this context and with a retrospective emphasis on “relatively,” we suggested that “Ideally, it might be desirable to conduct separate selection experiments on a long-standing equilibrium population and on a population derived relatively recently from the field.”  Lawrence G. Harshman School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68588-0118, USA (lharsh@unlserve.unl.edu)  Ary A. Hoffmann Department of Genetics and Evolution, La Trobe University, Bundoora, Victoria 3983, Australia (genaah@gen.latrobe.edu.au)  References  1. Lauder, G. V., et al. (1993) Adaptations and history. Trends Ecol. Evol. 8, 294–297. C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  4 2. Leroi, A. M., et al. (1994) What does the comparative method reveal about adaptation? Am. Nat. 143, 381–402. 3. Rose, M. R., et al. (1996) Laboratory evolution: the experimental wonderland and the Cheshire cat syndrome. In Adaptation (Rose, M. R., and Lauder, G. V., eds.), pp. 221–241, Academic Press. 4. Harshman, L. G., and Hoffmann, A. A. (2000) Laboratory selection experiments using Drosophila: what do they really tell us? Trends Ecol. Evol. 15, 32–36. 5. Matos, M., et al. (2000) An evolutionary no man’s land. Trends Ecol. Evol. 15, 206. 6. Frankham, R., and Loebel, D. A. (1992) Modeling problems in conservation genetics using cap-tive Drosophila populations: rapid genetic adaptation to captivity. Zool. Biol. 11, 333–342. 7. Matos, M., et al. (2000) Adaptation to the laboratory environment in Drosophila subobscura. J. Evol. Biol. 13, 9–19. 

An Evolutionary No Man’s Land  and  Reply from L. G. Harshman and A. A. Hoffmann

UNL | Libraries

University of Nebraska - Lincoln
DigitalCommons@University of Nebraska - Lincoln
Lawrence G. Harshman Publications Papers in the Biological Sciences
5-2000
"An Evolutionary No Man’s Land" and "Reply from
L. G. Harshman and A. A. Hoffmann"
Margarida Matos
Faculdade de Ciências de Lisboa, mmatos@fc.ul.pt
André Levy
State University of New York, Stony Brook, andrec@life.bio.sunysb.edu
Henrique Teotónio
University of California, Irvine, teotonio@uci.edu
Michael R. Rose
University of California, Irvine, mmrose@uci.edu
Lawrence G. Harshman
University of Nebraska–Lincoln, lharshman1@unl.edu
See next page for additional authors
Follow this and additional works at: http://digitalcommons.unl.edu/biosciharshman
Part of the Entomology Commons, and the Genetics Commons
This Letter to the Editor is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of
Nebraska - Lincoln. It has been accepted for inclusion in Lawrence G. Harshman Publications by an authorized administrator of
DigitalCommons@University of Nebraska - Lincoln.
Matos, Margarida; Levy, André; Teotónio, Henrique; Rose, Michael R.; Harshman, Lawrence G.; and Hoffmann, Ary A., ""An
Evolutionary No Man’s Land" and "Reply from L. G. Harshman and A. A. Hoffmann"" (2000). Lawrence G. Harshman Publications. 28.
http://digitalcommons.unl.edu/biosciharshman/28
Authors
Margarida Matos, André Levy, Henrique Teotónio, Michael R. Rose, Lawrence G. Harshman, and Ary A.
Hoffmann
This letter to the editor is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/
biosciharshman/28
 
 
 
Published in Correspondence, Trends in Ecology and Evolution 15:5 (May 2000), pp. 206, 207. 
Copyright © 2000 Elsevier Science Ltd. Used by permission. 
An Evolutionary No Man’s Land 
The gap between evolutionary studies in laboratory versus natural populations is a persis-
tent problem.1,2 In an attempt to bridge this gap, some researchers in the early 1980s stud-
ied the quantitative genetics of laboratory populations recently founded from the wild, 
with and without inbreeding.3,4 The dangers of such approaches were soon demonstrated 
experimentally.5,6 Inbreeding depression and genotype-by-environment interactions make 
such studies unreliable guides to the evolution of populations long-established in any en-
vironment. This conclusion is reiterated to some extent in Harshman and Hoffmann’s re-
cent TREE perspective,2 where the authors state that “The nature of laboratory selection 
regimes is unnatural.” But, they then go on to propose complementing selection experi-
ments in long-established laboratory populations with selection experiments in recently 
introduced ones. It is not clear how one could disentangle the causes of possible differences 
from the results of such disparate studies. Furthermore, from first principles and extant 
experimental studies, we expect a conflation of evolutionary effects in the recently intro-
duced populations because of adaptation to the laboratory environment, and because of 
genetic and evolutionary disequilibrium. In particular, interactions between adaptation to 
the general laboratory environment and any particular selective regime under study could 
be a source of unresolvable evolutionary outcomes, as we will now explain. 
Two evolutionary processes are at work in the transition from the wild to the laboratory. 
First, placing a population in a novel environment can cause a change in genetic variances 
and covariances between traits, as a result of genotype-by-environment interactions. Sec-
ond, continued maintenance in this novel environment might bring about evolutionary 
change, perhaps because of new selection pressures or changes in breeding structure. A 
recently founded laboratory population will thus be in a “no man’s land.” We cannot use 
it to provide information about the original wild population, nor can we test evolutionary 
models that rely on the assumption that the newly transplanted population is near genetic 
or selective equilibrium. Surprisingly, like Harshman and Hoffmann, several recent stud-
ies have essentially repeated these mistakes.7–9 
Let us conclude with an example. The empirical challenge posed by the transition from 
wild to laboratory conditions led us to study the evolution of a newly founded laboratory 
population of Drosophila subobscura.10 We found that adaptation to the novel, laboratory 
environment occurred at a relatively fast rate. As an illustration, fecundity around the age 
of reproduction increased steadily in the generations after establishment in the laboratory, 
showing convergence to the values of a long-established population serving as a control 
C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  
2 
(maintained in the lab for 24 generations before the foundation of the new one); the fecun-
dity of the new population became similar to that of the long-established population after 
just 14 generations of adaptation to the laboratory. In this no man’s land between the wild 
and the laboratory, the population evolved extremely rapidly. Instead of straining for du-
bious interpretations of the uncertain results afforded by studies of recently sampled pop-
ulations, we might use the gap between the wild and the laboratory as an evolutionary 
tool—recognizing that, after all, the lab is just another environment to which populations 
adapt, albeit a very peculiar one.10 To this extent, we can agree with Harshman and Hoff-
mann. 
 
Margarida Matos Carla Rego 
Centro de Biologia Ambiental, Departamento de Zoologia e Antropologia, Faculdade de Ciências 
de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal (mmatos@fc.ul.pt; crego@fc.ul.pt) 
 
André Levy 
Department of Ecology and Evolution, State University of New York, Stony Brook, NY 11794-5245, 
USA (andrec@life.bio.sunysb.edu) 
 
Henrique Teotónio 
Michael R. Rose 
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525, 
USA (teotonio@uci.edu; mrrose@uci.edu) 
 
References 
 
1. Rose, M. R., and Lauder, G. V., eds. (1996) Adaptation, Academic Press. 
2. Harshman, L. G., and Hoffmann, A. A. (2000) Laboratory selection experiments using Drosophila: 
what do they really tell us? Trends Ecol. Evol. 15, 32–36. 
3. Dingle, H., and Hegmann, J.,P., eds. (1982) Evolution and Genetics of Life Histories, Springer-Verlag. 
4. Giesel, J. T. (1986) Genetic correlation structure of life history variables in outbred, wild Drosoph-
ila melanogaster : effects of photoperiod regimen. Am. Nat. 128, 593–603. 
5. Rose, M. R. (1984) Genetic covariation in Drosophila life history: untangling the data. Am. Nat. 
123, 565–569. 
6. Service, P. M., and Rose, M. R. (1985) Genetic covariation among life-history components: the 
effect of novel environments. Evolution 39, 943–945. 
7. Blanckenhorn, W. U., et al. (1998) Fluctuating asymmetry, body size, and sexual selection in the 
dung fly Sepsis cynipsea—testing the good genes assumptions and predictions. J. Evol. Biol. 11, 
735–753. 
8. Reusch, T., and Blanckenhorn, W. U. (1998) Quantitative genetics of the dung fly Sepsis cynipsea: 
Cheverud’s conjecture revisited. Heredity 81, 111–119. 
9. Windig, J. J. (1999) Trade-offs between melanization, development time, and adult size in Inachis 
io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity 82, 57–68. 
10. Matos, M., et al. (2000) Adaptation to the laboratory environment in Drosophila subobscura. J. 
Evol. Biol. 13, 9–19. 
C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  
3 
Reply from L. G. Harshman and 
A. A. Hoffmann 
It has been argued that laboratory evolution experiments are superior to comparative stud-
ies1,2 and phenotypic manipulations3 for the study of evolution. It has also been argued 
that there are constraints on the design of most field evolution studies compared with la-
boratory evolution experiments,3 and suggested that interpreting the results of field evo-
lutionary studies is problematical relative to laboratory evolution experiments.3 However, 
a crucial perspective on laboratory evolution studies calls these points of view into ques-
tion. As we discussed in our recent TREE article,4 there is a range of problems associated 
with laboratory selection experiments using Drosophila to study the evolution of life history 
and stress-related traits. In their letter, Matos et al.5 did not significantly address any of the 
issues we raised.4 
Their reply5 is a bit puzzling because their argument is similar to the one we presented.4 
Like us, they describe the problem associated with conducting selection experiments using 
populations recently established in the laboratory. Specifically, we stated that “There is 
some evidence that Drosophila can adapt rapidly to laboratory culture,6 reducing the con-
cern about using populations maintained in the laboratory for only a short term. Never-
theless, it is unclear how many generations are required to dampen any spurious 
correlations potentially generated by domestication. To illuminate this issue, it is im-
portant to investigate the process of Drosophila domestication in terms of the time course 
of changes in life history and of stress-related traits, and to investigate the patterns of ge-
netic correlations among traits.”7 Once we have such information, it can be used as a basis 
to decide how long to maintain populations in the laboratory before initiating selection 
experiments; recommendations can be made about any likely confounding effects; and 
general guidelines could be established for comparing recently established and long-
established populations. In this context and with a retrospective emphasis on “relatively,” 
we suggested that “Ideally, it might be desirable to conduct separate selection experiments 
on a long-standing equilibrium population and on a population derived relatively recently 
from the field.” 
 
Lawrence G. Harshman 
School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68588-0118, USA 
(lharsh@unlserve.unl.edu) 
 
Ary A. Hoffmann 
Department of Genetics and Evolution, La Trobe University, Bundoora, Victoria 3983, Australia 
(genaah@gen.latrobe.edu.au) 
 
References 
 
1. Lauder, G. V., et al. (1993) Adaptations and history. Trends Ecol. Evol. 8, 294–297. 
C O R R E S P O N D E N C E ,  T R E N D S  I N  E C O L O G Y  A N D  E V O L U T I O N  1 5  (2 0 00 )  
4 
2. Leroi, A. M., et al. (1994) What does the comparative method reveal about adaptation? Am. Nat. 
143, 381–402. 
3. Rose, M. R., et al. (1996) Laboratory evolution: the experimental wonderland and the Cheshire 
cat syndrome. In Adaptation (Rose, M. R., and Lauder, G. V., eds.), pp. 221–241, Academic Press. 
4. Harshman, L. G., and Hoffmann, A. A. (2000) Laboratory selection experiments using Drosophila: 
what do they really tell us? Trends Ecol. Evol. 15, 32–36. 
5. Matos, M., et al. (2000) An evolutionary no man’s land. Trends Ecol. Evol. 15, 206. 
6. Frankham, R., and Loebel, D. A. (1992) Modeling problems in conservation genetics using cap-
tive Drosophila populations: rapid genetic adaptation to captivity. Zool. Biol. 11, 333–342. 
7. Matos, M., et al. (2000) Adaptation to the laboratory environment in Drosophila subobscura. J. 
Evol. Biol. 13, 9–19. 


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An Evolutionary No Man’s Land and Reply from L. G. Harshman and A. A. Hoffmann

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