Reversed selection responses in small populations of the housefly (Musca domestica L.)
We compared the efficacy of artificial and natural selection processes in purging the genetic load of perpetually small populations. We subjected replicate lines of the housefly (Musca domestica L.), recently derived from the wild, to artificial selection for increased mating propensity (i.e., the proportion of male–female pairs initiating copulation within 30 min) in efforts to cull out the inbreeding depression effects of long-term small population size (as determined by a selection protocol for increased assortative mating). We also maintained parallel non-selection lines for assessing the spontaneous purge of genetic load due to inbreeding alone. We thus evaluated the fitness of artificially and ‘naturally’ purging populations held at census sizes of 40 individuals over the course of 18 generations. We found that the artificially selected lines had significant increases in mating propensity (up to 46% higher from the beginning of the protocol) followed by reversed selection responses back to the initial levels, resulting in non-significant heritabilities. Nevertheless, the ‘naturally’ selected lines had significantly lower fitness overall (a 28% reduction from the beginning of the protocol), although lower effective population sizes could have contributed to this effect. We conclude that artificial selection bolstered fitness, but only in the short-term, because the inadvertent fixation of extant genetic load later resulted in pleiotropic fitness declines. Still, the short-term advantage of the selection protocol likely contributed to the success of the speciation experiment since our recently-derived housefly populations are particularly vulnerable to inbreeding depression effects on mating behavior.
Keywordsartificial selection genetic load mating behavior pleiotropy purge
Ballou, J.D. 1997Ancestral inbreeding only minimally affects inbreeding depression in mammalian populationsJ. Hered.88169178PubMedGoogle Scholar Bijlsma, R., Bundgaard, J., Boerema, A.C. 2000Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila J. Evol. Biol.13502514CrossRefGoogle Scholar Bijlsma, R., Bundgaard, J., Putten, W.F. 1999Environmental dependence of inbreeding depression and purging in Drosophila melanogaster J. Evol. Biol.1211251137CrossRefGoogle Scholar Brewer, B.A., Lacy, R.C., Foster, M.L., Alaks, G. 1990Inbreeding depression in insular and central populations of Peromyscus miceJ. Hered.81257266PubMedGoogle Scholar Bryant, E.H., Meffert, L.M., McCommas, S.A. 1990Fitness rebound in serially bottlenecked populations of the house flyAm. Nat.136543549CrossRefGoogle Scholar Bulmer, M.G. 1971The effect of selection on genetic variabilityAm. Nat.105201211CrossRefGoogle Scholar Burnet, B., Connolly, K. 1974Activity and sexual behaviour in Drosophila melanogasterAbeelen, J.H.F. eds. The Genetics of BehaviourNorth-Holland PublishingThe Netherlands201258. Google Scholar Byers, D.L., Waller, D.M. 1999Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depressionAnnu. Rev. Ecol. Syst.30479513CrossRefGoogle Scholar Caballero, A., Toro, M.A., López-Fanjul, C. 1991The response to artificial selection from new mutations in Drosophila melanogaster Genetics12789102Google Scholar Charlesworth, B. 1998The effect of synergistic epistasis on the inbreeding loadGenet. Res. Camb.718589Google Scholar Charlesworth, B., Charlesworth, D. 1987Inbreeding depression and its evolutionary consequencesAnnu. Rev. Ecol. Syst.18237268CrossRefGoogle Scholar Crnokrak, P., Barrett, S.C.H. 2002Perspective: purging the genetic load: a review of the experimental evidenceEvolution5623472358PubMedCrossRefGoogle Scholar Crow, J.F. 1993Mutation, mean fitness, and genetic loadFutuyma, D.Antonovics, J. eds. in Oxford Surveys in Evolutionary BiologyOxford University PressOxford342Google Scholar
Crow, J.F. & N.E. Morton, 1955. Measurement of gene frequency drift in small populations. Evolution : 202–214.Google Scholar
Day, S.B., Bryant, E.H., Meffert, L.M. 2003The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potentialEvolution5713141324PubMedCrossRefGoogle Scholar Dudash, M.R., Carr, D.E., Fenster, C.B. 1997Five generations of enforced selfing and outcrossing in Mimulus guttatus: inbreeding depression variation at the population and family levelEvolution515465CrossRefGoogle Scholar Falconer, D.S. 1989Introduction to Quantitative Genetics2nd edn. LongmanNew YorkGoogle Scholar Faugeres, A., Petit, C., Thibout, E. 1971The components of sexual selectionEvolution25265275CrossRefGoogle Scholar Frankham, R. 1995aInbreeding and extinction: a threshold effectConserv. Biol.9792799CrossRefGoogle Scholar Frankham, R. 1995bConservation geneticsAnnu. Rev. Genet.29305327CrossRefGoogle Scholar Frankham, R., Gilligan, D.M., Morris, D., Briscoe, D.A. 2001Inbreeding and extinction: effects of purgingConserv. Genet.2279285CrossRefGoogle Scholar Frankham, R., Yoo, B.H., Sheldon, B.L. 1988Reproductive fitness and artificial selection in animal breeding: culling on fitness prevents a decline in reproductive fitness in lines of Drosophila melanogaster selected for increased inebriation timeTheor. Appl. Genet.76909914CrossRefGoogle Scholar García, N., López-Fanjul, C., García-Dorado, A. 1994The genetics of viability in Drosophila melanogaster: effects of inbreeding and artificial selectionEvolution4812771285CrossRefGoogle Scholar Hedrick, P.W. 1994Purging inbreeding depression and the probability of extinction: full-sib matingJ. Hered.73363372Google Scholar Hill, W.G., Caballero, A. 1992Artificial selection experimentsAnnu. Rev. Ecol. Syst.23287310CrossRefGoogle Scholar Hollingsworth, M.J., Maynard Smith, J. 1955The effects of inbreeding on rate of development and on fertility in Drosophila subobscura J. Genet.53295314CrossRefGoogle Scholar Keightley, P.D., Hill, W.G. 1992Quantitative genetic variation in body size of mice from new mutationsGenetics131693700PubMedGoogle Scholar Kondrashov, A.S. 1995Contamination of the genome by very slightly deleterious mutations: why have we not died 100 times over?J. Theor. Biol.175583594PubMedCrossRefGoogle Scholar Lacy, R.L., Alaks, G., Walsh, A. 1996Hierarchical analysis of inbreeding depression in Peromyscus polionotus Evolution5021872200CrossRefGoogle Scholar Lacy, R.C., Ballou, J.D. 1998Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreedingEvolution52900909CrossRefGoogle Scholar Lande, R. 1994Risk of population extinction from new deleterious mutationsEvolution4814601469CrossRefGoogle Scholar Lande, R. 1995Mutation and conservationConserv. Biol.9782791CrossRefGoogle Scholar Lande, R., Schemske, D.W., Schultz, S.T. 1994High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutationsEvolution48965978CrossRefGoogle Scholar Latter, B.D.H., Mulley, J.C. 1995Genetic adaptation to captivity and inbreeding depression in small laboratory populations of Drosophila melanogaster Genetics139255266PubMedGoogle Scholar Latter, B.D.H., Mulley, J.C., Reid, D., Pascoe, L. 1995Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster Genetics139287297PubMedGoogle Scholar López, M., López-Fanjul, C. 1993Spontaneous mutation for a quantitative trait in Drosophila melanogaster Genet. Res. Camb.61107116Google Scholar López-Fanjul, C., Fernandez, A., Toro, M.A. 2000Epistasis and the conversion of non-additive genetic variance at population bottlenecksTheor. Popul. Biol.584959PubMedCrossRefGoogle Scholar López-Fanjul, C., Villaverde, A. 1989Inbreeding increases genetic variance for viability in Drosophila melanogaster Evolution4318001804CrossRefGoogle Scholar Lynch, M., Connery, J., Bürger, R. 1995Mutational meltdowns in sexual populationsEvolution4910671080CrossRefGoogle Scholar Markow, T.A. 1981Courtship behavior and control of reproductive isolation between Drosophila mojavensis and Drosophila arizonensis Evolution3510221026CrossRefGoogle Scholar McCall, D., Waller, M., Mitchell-Olds, T. 1994Effects of serial inbreeding on fitness components in Impatiens capensis Evolution48818827CrossRefGoogle Scholar Meffert, L.M., Bryant, E.H. 1991Mating propensity and courtship behavior in serially bottlenecked lines of the houseflyEvolution45293306CrossRefGoogle Scholar Meffert, L.M., Bryant, E.H. 1992Divergent ambulatory and grooming behavior in serially bottlenecked lines of the houseflyEvolution4613991407CrossRefGoogle Scholar Meffert, L.M., Regan, J.L. 2002A test of speciation via sexual selection on female preferencesAnim. Behav.64955965CrossRefGoogle Scholar Meffert, L.M., Regan, J.L., Brown, B.W. 1999Convergent evolution of the mating behaviour of founder-flush populations of the houseflyJ. Evol. Biol.12859868CrossRefGoogle Scholar Miller, P.S., Hedrick, P.W. 2001Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster J. Evol. Biol.14595601CrossRefGoogle Scholar Mooers, A.Ø., Rundle, H.D., Whitlock, M.C. 1999The effects of selection and bottlenecks on male mating success in peripheral isolatesAm. Nat.153437444CrossRefGoogle Scholar Parsons, P.A. 1974Mating speed as a component of fitness in Drosophila Behav. Genet.4395404PubMedCrossRefGoogle Scholar Poon, A., Otto, S.P. 2000Compensating for our load of mutations: freezing the meltdown of small populationsEvolution5414671479PubMedCrossRefGoogle Scholar Reed, D., Bryant, E.H. 2001Fitness, genetic load and purging in experimental populations of the houseflyConserv. Genet.25762CrossRefGoogle Scholar Reed, D.H., Lowe, E.H., Briscoe, D.A., Frankham, R. 2003Inbreeding and extinction: effects of rate of inbreedingConserv. Genet.4405410CrossRefGoogle Scholar Regan, J.L., Meffert, L.M., Bryant, E.H. 2003A direct experimental test of founder-flush effects on the evolutionary potential for assortative matingJ. Evol. Biol.16302312PubMedCrossRefGoogle Scholar Robertson, A. 1952The effect of inbreeding on the variation due to recessive genesGenetics37189207PubMedGoogle Scholar Rodríguez-Ramilo, S.T., Pérez-Figeroa, A., Fernández, B., Fernandez, J., Caballero, A. 2004Mutation-selection balance accounting for genetic variation for viability in Drosophila melanogaster as deduced from an inbreeding and artificial selection experimentJ. Evol. Biol.17528541PubMedCrossRefGoogle Scholar Rose, M.R. 1984Artificial selection on a fitness component in Drosophila melanogaster Evolution38516526CrossRefGoogle Scholar Saccheri, I.J., Brakefield, P.M., Nichols, R.A. 1996Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae)Evolution5020002013CrossRefGoogle Scholar
SAS 1988. SAS Institute, Inc. Cary, North CarolinaGoogle Scholar
Schultz, S., Lynch, M. 1997Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossingEvolution5113631371CrossRefGoogle Scholar Sharp, P.M. 1984The effect of inbreeding on competitive male-mating ability in Drosophila melanogaster Genetics106601612PubMedGoogle Scholar Spielman, D., Frankham, R. 1992Modeling problems in conservation genetics using captive Drosophila populations: improvement of reproductive fitness due to immigration of one individual into small partially inbred populationsZoo. Biol.11343351CrossRefGoogle Scholar Thornhill, N.W. 1993The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical PerspectivesUniversity of Chicago PressChicagoGoogle Scholar Oosterhout, C., Smit, G., Heuven, M.K., Brakefield, P.M. 2000aPedigree analysis on small laboratory populations of the butterfly Bicyclus anynana: the effects of selection on inbreeding and fitnessConserv. Genet.4321328CrossRefGoogle Scholar Oosterhout, C., Zijlstra, W.G., Heuven, M.K., Brakefield, P.M. 2000bInbreeding depression and genetic load in laboratory populations of the butterfly Bicyclus anynana Evolution54218225CrossRefGoogle Scholar Wade, M.J., Shuster, S.M., Stevens, L. 1996Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum Evolution50723733CrossRefGoogle Scholar Wang, J. 2000Effects of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutationsGenet. Res. Camb.767586Google Scholar Wang, J., Hill, W.G., Charlesworth, D., Charlesworth, B. 1999Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rateGenet. Res. Camb.74165178Google Scholar Whitlock, M.C. 2000Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selectionEvolution5418551861PubMedCrossRefGoogle Scholar Whitlock, M.C., Phillips, P.C., Wade, M.J. 1993Gene interaction affects the additive genetic variance in subdivided populations with migration and extinctionEvolution4717581769CrossRefGoogle Scholar Willis, J.H., Orr, H.A. 1993Increased heritable variation following population bottlenecks: the role of dominanceEvolution47949956CrossRefGoogle Scholar