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Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus Neurospora.

Dettman JR, Anderson JB, Kohn LM - BMC Evol. Biol. (2008)

Bottom Line: The effects of divergent adaptation on reproductive isolation were more pronounced for populations with greater initial genetic variation.When brought together by mating, these alleles interacted negatively and had detrimental effects on sexual reproductive success, in agreement with the Dobzhansky-Muller model of genetic incompatibilities.These results support that, given adequate standing genetic variation, divergent adaptation can indirectly cause the evolution of reproductive isolation, and eventually lead to speciation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, L5L 1C6, Canada. jeremy.dettman@utoronto.ca

ABSTRACT

Background: An open, focal issue in evolutionary biology is how reproductive isolation and speciation are initiated; elucidation of mechanisms with empirical evidence has lagged behind theory. Under ecological speciation, reproductive isolation between populations is predicted to evolve incidentally as a by-product of adaptation to divergent environments. The increased genetic diversity associated with interspecific hybridization has also been theorized to promote the development of reproductive isolation among independent populations. Using the fungal model Neurospora, we founded experimental lineages from both intra- and interspecific crosses, and evolved them in one of two sub-optimal, selective environments. We then measured the influence that initial genetic diversity and the direction of selection (parallel versus divergent) had on the evolution of reproductive isolation.

Results: When assayed in the selective environment in which they were evolved, lineages typically had greater asexual fitness than the progenitors and the lineages that were evolved in the alternate, selective environment. Assays for reproductive isolation showed that matings between lineages that were adapted to the same environment had greater sexual reproductive success than matings between lineages that were adapted to different environments. Evidence of this differential reproductive success was observed at two stages of the sexual cycle. For one of the two observed incompatibility phenotypes, results from genetic analyses were consistent with a two-locus, two-allele model with asymmetric (gender-specific), antagonistic epistasis. The effects of divergent adaptation on reproductive isolation were more pronounced for populations with greater initial genetic variation.

Conclusion: Divergent selection resulted in divergent adaptation and environmental specialization, consistent with fixation of different alleles in different environments. When brought together by mating, these alleles interacted negatively and had detrimental effects on sexual reproductive success, in agreement with the Dobzhansky-Muller model of genetic incompatibilities. As predicted by ecological speciation, greater reproductive isolation was observed among divergent-adapted lineages than among parallel-adapted lineages. These results support that, given adequate standing genetic variation, divergent adaptation can indirectly cause the evolution of reproductive isolation, and eventually lead to speciation.

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Progeny viability in the permissive environment for matings in Experiment L (a) and Experiment H (b). Matings in which the female lineage was fertilized by males evolved in the parallel environment (PE matings, n = 12) or the divergent environment (DE matings, n = 18), are in grey or white, respectively. For clarity, the paternal lineage-classes are also shown. Asterisks indicate significance differences between mating classes, as determined by Fisher exact tests (two-tailed) using ascospore germination/non-germination frequencies. Mean n per maternal lineage-class > 3360 ascospores scored. Errors bars are standard error.
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Figure 4: Progeny viability in the permissive environment for matings in Experiment L (a) and Experiment H (b). Matings in which the female lineage was fertilized by males evolved in the parallel environment (PE matings, n = 12) or the divergent environment (DE matings, n = 18), are in grey or white, respectively. For clarity, the paternal lineage-classes are also shown. Asterisks indicate significance differences between mating classes, as determined by Fisher exact tests (two-tailed) using ascospore germination/non-germination frequencies. Mean n per maternal lineage-class > 3360 ascospores scored. Errors bars are standard error.

Mentions: In general, progeny viability was greater when females were fertilized by males evolved in the parallel environment than when fertilized by males evolved in the divergent environment. These differences were significant at both assay points for one of the two lineage classes in each experiment: the LT and HN lineage classes in Exp. L and H, respectively (Fig. 4). These patterns were shared among lineages within lineage classes: PE > DE matings for all three LT and HN lineages (data not shown). In addition, PE matings were significantly more successful than DE matings for 5 of the assay points along the course of evolution (data not shown, Fisher exact tests; LT, p ≤ 0.0004 in each case; HN, p < 0.0001 in each case), demonstrating a clear trend through time.


Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus Neurospora.

Dettman JR, Anderson JB, Kohn LM - BMC Evol. Biol. (2008)

Progeny viability in the permissive environment for matings in Experiment L (a) and Experiment H (b). Matings in which the female lineage was fertilized by males evolved in the parallel environment (PE matings, n = 12) or the divergent environment (DE matings, n = 18), are in grey or white, respectively. For clarity, the paternal lineage-classes are also shown. Asterisks indicate significance differences between mating classes, as determined by Fisher exact tests (two-tailed) using ascospore germination/non-germination frequencies. Mean n per maternal lineage-class > 3360 ascospores scored. Errors bars are standard error.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2270261&req=5

Figure 4: Progeny viability in the permissive environment for matings in Experiment L (a) and Experiment H (b). Matings in which the female lineage was fertilized by males evolved in the parallel environment (PE matings, n = 12) or the divergent environment (DE matings, n = 18), are in grey or white, respectively. For clarity, the paternal lineage-classes are also shown. Asterisks indicate significance differences between mating classes, as determined by Fisher exact tests (two-tailed) using ascospore germination/non-germination frequencies. Mean n per maternal lineage-class > 3360 ascospores scored. Errors bars are standard error.
Mentions: In general, progeny viability was greater when females were fertilized by males evolved in the parallel environment than when fertilized by males evolved in the divergent environment. These differences were significant at both assay points for one of the two lineage classes in each experiment: the LT and HN lineage classes in Exp. L and H, respectively (Fig. 4). These patterns were shared among lineages within lineage classes: PE > DE matings for all three LT and HN lineages (data not shown). In addition, PE matings were significantly more successful than DE matings for 5 of the assay points along the course of evolution (data not shown, Fisher exact tests; LT, p ≤ 0.0004 in each case; HN, p < 0.0001 in each case), demonstrating a clear trend through time.

Bottom Line: The effects of divergent adaptation on reproductive isolation were more pronounced for populations with greater initial genetic variation.When brought together by mating, these alleles interacted negatively and had detrimental effects on sexual reproductive success, in agreement with the Dobzhansky-Muller model of genetic incompatibilities.These results support that, given adequate standing genetic variation, divergent adaptation can indirectly cause the evolution of reproductive isolation, and eventually lead to speciation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, L5L 1C6, Canada. jeremy.dettman@utoronto.ca

ABSTRACT

Background: An open, focal issue in evolutionary biology is how reproductive isolation and speciation are initiated; elucidation of mechanisms with empirical evidence has lagged behind theory. Under ecological speciation, reproductive isolation between populations is predicted to evolve incidentally as a by-product of adaptation to divergent environments. The increased genetic diversity associated with interspecific hybridization has also been theorized to promote the development of reproductive isolation among independent populations. Using the fungal model Neurospora, we founded experimental lineages from both intra- and interspecific crosses, and evolved them in one of two sub-optimal, selective environments. We then measured the influence that initial genetic diversity and the direction of selection (parallel versus divergent) had on the evolution of reproductive isolation.

Results: When assayed in the selective environment in which they were evolved, lineages typically had greater asexual fitness than the progenitors and the lineages that were evolved in the alternate, selective environment. Assays for reproductive isolation showed that matings between lineages that were adapted to the same environment had greater sexual reproductive success than matings between lineages that were adapted to different environments. Evidence of this differential reproductive success was observed at two stages of the sexual cycle. For one of the two observed incompatibility phenotypes, results from genetic analyses were consistent with a two-locus, two-allele model with asymmetric (gender-specific), antagonistic epistasis. The effects of divergent adaptation on reproductive isolation were more pronounced for populations with greater initial genetic variation.

Conclusion: Divergent selection resulted in divergent adaptation and environmental specialization, consistent with fixation of different alleles in different environments. When brought together by mating, these alleles interacted negatively and had detrimental effects on sexual reproductive success, in agreement with the Dobzhansky-Muller model of genetic incompatibilities. As predicted by ecological speciation, greater reproductive isolation was observed among divergent-adapted lineages than among parallel-adapted lineages. These results support that, given adequate standing genetic variation, divergent adaptation can indirectly cause the evolution of reproductive isolation, and eventually lead to speciation.

Show MeSH