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Intragenomic conflict in populations infected by Parthenogenesis Inducing Wolbachia ends with irreversible loss of sexual reproduction.

Stouthamer R, Russell JE, Vavre F, Nunney L - BMC Evol. Biol. (2010)

Bottom Line: The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased.In haplodiploid species a reduced fertilization rate leads to the production of more sons.This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, University of California, Riverside, CA 92521, USA. richard.stouthamer@ucr.edu

ABSTRACT

Background: The maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-Wolbachia in a previously uninfected population leads to a genomic conflict between PI-Wolbachia and the nuclear genome. In most natural populations infected with PI-Wolbachia the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.

Results: The PI Wolbachia infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-Wolbachia infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-Wolbachia infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.

Conclusions: This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

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Related in: MedlinePlus

Mutant fertilization alleles can invade PI-Wolbachia infected populations even when they have a negative fitness effect in the homozygous state. When homozygosity for the recessive mutant allele n with a fertilization rate of m also carries a cost (s), the mutation can spread from rarity as long as the cost of homozygosity for the mutant and the fertilization frequency of the mutant within in the single hatched (simulation results) or in the double hatched area (simulation and analytical results). The mutant fertilization rate competes with a wildtype fertilization rate of x = 0.5. Other values: no cost of being infected (ω = 1), the Wolbachia transmission efficiency (α) equals 0.95.
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Figure 6: Mutant fertilization alleles can invade PI-Wolbachia infected populations even when they have a negative fitness effect in the homozygous state. When homozygosity for the recessive mutant allele n with a fertilization rate of m also carries a cost (s), the mutation can spread from rarity as long as the cost of homozygosity for the mutant and the fertilization frequency of the mutant within in the single hatched (simulation results) or in the double hatched area (simulation and analytical results). The mutant fertilization rate competes with a wildtype fertilization rate of x = 0.5. Other values: no cost of being infected (ω = 1), the Wolbachia transmission efficiency (α) equals 0.95.

Mentions: So far we have assumed that the mutations are neutral with respect to offspring production. In many cases it could be argued that mutations interfering with the fertilization behavior would indeed be neutral or even have a fitness advantage for females. For instance, if the mutation interferes with costly traits involved with sexual reproduction such as pheromone production or storage of sperm etc., the resources that otherwise would have been spent on these traits may become available for other life history traits, resulting in higher offspring production by mutant females. A positive fitness effect of homozygosity for the fertilization mutant allows the mutation to spread more rapidly through the population. However, even a negative fitness effect of homozygosity for the fertilization mutation does not preclude its spread. Using our simulation model (additional file 1) we show in Figure 6 the conditions under which a sex ratio mutant, which when homozygous has a negative fitness effect on its host, is still capable of invading a population with a spreading PI-Wolbachia infection. Figure 6 also shows that the simulation results are consistent with the results from our analytic model (eqn A4, additional file 2). The analytic result is consistently slightly more restrictive. This minor difference may be due to the analytic result assumes the spread of the fertilization mutation is only driven by the Inn females producing males carrying the mutant allele, while there is at least initially also a small contribution from heterozygous infected and uninfected females.


Intragenomic conflict in populations infected by Parthenogenesis Inducing Wolbachia ends with irreversible loss of sexual reproduction.

Stouthamer R, Russell JE, Vavre F, Nunney L - BMC Evol. Biol. (2010)

Mutant fertilization alleles can invade PI-Wolbachia infected populations even when they have a negative fitness effect in the homozygous state. When homozygosity for the recessive mutant allele n with a fertilization rate of m also carries a cost (s), the mutation can spread from rarity as long as the cost of homozygosity for the mutant and the fertilization frequency of the mutant within in the single hatched (simulation results) or in the double hatched area (simulation and analytical results). The mutant fertilization rate competes with a wildtype fertilization rate of x = 0.5. Other values: no cost of being infected (ω = 1), the Wolbachia transmission efficiency (α) equals 0.95.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2927591&req=5

Figure 6: Mutant fertilization alleles can invade PI-Wolbachia infected populations even when they have a negative fitness effect in the homozygous state. When homozygosity for the recessive mutant allele n with a fertilization rate of m also carries a cost (s), the mutation can spread from rarity as long as the cost of homozygosity for the mutant and the fertilization frequency of the mutant within in the single hatched (simulation results) or in the double hatched area (simulation and analytical results). The mutant fertilization rate competes with a wildtype fertilization rate of x = 0.5. Other values: no cost of being infected (ω = 1), the Wolbachia transmission efficiency (α) equals 0.95.
Mentions: So far we have assumed that the mutations are neutral with respect to offspring production. In many cases it could be argued that mutations interfering with the fertilization behavior would indeed be neutral or even have a fitness advantage for females. For instance, if the mutation interferes with costly traits involved with sexual reproduction such as pheromone production or storage of sperm etc., the resources that otherwise would have been spent on these traits may become available for other life history traits, resulting in higher offspring production by mutant females. A positive fitness effect of homozygosity for the fertilization mutant allows the mutation to spread more rapidly through the population. However, even a negative fitness effect of homozygosity for the fertilization mutation does not preclude its spread. Using our simulation model (additional file 1) we show in Figure 6 the conditions under which a sex ratio mutant, which when homozygous has a negative fitness effect on its host, is still capable of invading a population with a spreading PI-Wolbachia infection. Figure 6 also shows that the simulation results are consistent with the results from our analytic model (eqn A4, additional file 2). The analytic result is consistently slightly more restrictive. This minor difference may be due to the analytic result assumes the spread of the fertilization mutation is only driven by the Inn females producing males carrying the mutant allele, while there is at least initially also a small contribution from heterozygous infected and uninfected females.

Bottom Line: The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased.In haplodiploid species a reduced fertilization rate leads to the production of more sons.This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, University of California, Riverside, CA 92521, USA. richard.stouthamer@ucr.edu

ABSTRACT

Background: The maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-Wolbachia in a previously uninfected population leads to a genomic conflict between PI-Wolbachia and the nuclear genome. In most natural populations infected with PI-Wolbachia the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.

Results: The PI Wolbachia infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-Wolbachia infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-Wolbachia infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.

Conclusions: This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

Show MeSH
Related in: MedlinePlus