Evol Ecol Res 14: 403-423 (2012)     Full PDF if your library subscribes.

Drift and selection entwined: asymmetric reproductive isolation in an experimental niche shift

Jay J. Falk1, Christine E. Parent1,2, Deepa Agashe3* and Daniel I. Bolnick4

1Section of Integrative Biology, University of Texas at Austin, Austin, Texas, USA, 2Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, California, USA,  3Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA and  4Howard Hughes Medical Institute and Section of Integrative Biology, University of Texas at Austin, Austin, Texas, USA

Correspondence: J.J. Falk, Section of Integrative Biology, One University Station C0930, University of Texas at Austin, Austin, TX 78712, USA.
e-mail: j.jinsing@gmail.com


Question: Host races of phytophagous insects originate when a population adapts to a novel resource (host) while other populations remain resident on their ancestral host. The derived and ancestral host race populations will be subject to unequal selection intensity and genetic drift. Is this asymmetry responsible for asymmetric reproductive isolation observed in some populations?

Hypothesis: Unequal intensity of selection and/or genetic drift between populations may lead to asymmetric reproductive isolation.

Methods: We reared populations of Tribolium castaneum flour beetles on wheat or corn flour, which represent ancestral and suboptimal novel resources respectively. After approximately 43 generations, we assayed the fitness of wheat- and corn-evolved beetles on wheat and corn flour, and measured reciprocal pre-mating, pre-zygotic, and post-zygotic reproductive isolation between the ecotypes.

Results: Three of our four corn-evolved populations went extinct. The one surviving corn population exhibited evidence of adaptation to corn half way through the experiment, but by the final generation we found little evidence of adaptation. Instead, the corn-evolved population had lower survival than the wheat-evolved population, independent of rearing environment. This result is consistent with maladaptation due to fixation of deleterious alleles via genetic drift. Pre-mating and post-zygotic reproductive isolation were both asymmetric, favouring the higher-fitness ancestral population. Females from both wheat- and corn-evolved populations avoided mating with corn-evolved males. This bias improved female fitness, because corn-evolved males had offspring with lower survival, regardless of female genotype or rearing medium.

Conclusion: Strong selection in the derived (corn) population appears to have decreased population size to the extent that genetic drift led to the fixation of deleterious alleles that reduced corn-evolved male fitness. We posit that asymmetric pre-mating isolation arose because of this drift-induced maladaptation. Although our study is limited to a single pair of derived and ancestral populations, the results of our extensive pre- and post-mating reproductive isolation tests are consistent with this conclusion. This study highlights the importance of recognizing the fundamental entangling of drift and selection in the evolution of reproductive isolation, which complicates the frequently invoked dichotomy of selection and drift as distinct alternative forces in speciation.

Keywords: ecological speciation, founder effects, inbreeding depression, niche shift, phytophagous insects, post-zygotic isolation, pre-mating isolation, pre-zygotic isolation.

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