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Sexual versus Asexual Reproduction: Distinct Outcomes in Relative Abundance of Parthenogenetic Mealybugs following Recent Colonization.

Tabata J, Ichiki RT, Tanaka H, Kageyama D - PLoS ONE (2016)

Bottom Line: Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a "cost of males." Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations.Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage.This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.

View Article: PubMed Central - PubMed

Affiliation: National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan.

ABSTRACT
Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a "cost of males." Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations. But the evolution of sexual reproduction remains unclear, because we have limited examples that demonstrate the relative success of sexual lineages in the face of competition from asexual lineages in the same environment. Here we investigated a sympatric occurrence of sexual and asexual reproduction in the pineapple mealybug, Dysmicoccus brevipes. This pest invaded southwestern Japan, including Okinawa and Ishigaki Islands, in the 1930s in association with imported pineapple plants. Our recent censuses demonstrated that on Okinawa sexually reproducing individuals can coexist with and even dominate asexual individuals in the presence of habitat and resource competition, which is considered to be severe for this nearly immobile insect. Molecular phylogeny based on partial DNA sequences in the mitochondrial and nuclear genomes, as well as the endosymbiotic bacterial genome, revealed that the asexual lineage diverged from a common sexual ancestor in the relatively recent past. In contrast, only the asexual lineage exhibiting obligate apomictic thelytoky was discovered on Ishigaki. Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage. Differences in biotic and/or abiotic selective forces operating on the two islands might be the cause of this discrepancy. This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.

No MeSH data available.


Related in: MedlinePlus

Phylogeny of the sexual and asexual lineages based on partial sequences of mitochondria (CO1; a), an intracellular symbiont (rpoB; b), and the nuclear (ITS2; c) genome.The trees were constructed by the maximum likelihood method using unambiguously aligned nucleotide sites. The trees of rpoB and ITS2 are rooted on each midpoint. The bootstrap values (>50%) obtained from 1000 resamplings are given at the nodes. Sequences of the taxa with the DDBJ/EMBL/GenBank accession numbers in brackets were obtained from the database.
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pone.0156587.g003: Phylogeny of the sexual and asexual lineages based on partial sequences of mitochondria (CO1; a), an intracellular symbiont (rpoB; b), and the nuclear (ITS2; c) genome.The trees were constructed by the maximum likelihood method using unambiguously aligned nucleotide sites. The trees of rpoB and ITS2 are rooted on each midpoint. The bootstrap values (>50%) obtained from 1000 resamplings are given at the nodes. Sequences of the taxa with the DDBJ/EMBL/GenBank accession numbers in brackets were obtained from the database.

Mentions: Six haplotypes were found based on the mitochondrial CO1 sequences (1449 bp). These haplotypes were clearly divided into two groups corresponding to the sexual lineage and the asexual lineage (Fig 3a). Among the haplotypes of the sexual lineage, haplotype A1 was predominant (87.5%). In the asexual lineage, haplotype P1 was similarly predominant both on Okinawa (87.5%) and Ishigaki (66.7%). Each haplotype represented a group that was the most closely related among the CO1 sequences of all mealybug species examined and clustered into clades with high bootstrap values (Fig 3a). A total of 35 nucleotide sites were substituted (2.4%; 16 transitions and 19 transversions involving eight amino acid substitutions) between haplotypes A1 and P1.


Sexual versus Asexual Reproduction: Distinct Outcomes in Relative Abundance of Parthenogenetic Mealybugs following Recent Colonization.

Tabata J, Ichiki RT, Tanaka H, Kageyama D - PLoS ONE (2016)

Phylogeny of the sexual and asexual lineages based on partial sequences of mitochondria (CO1; a), an intracellular symbiont (rpoB; b), and the nuclear (ITS2; c) genome.The trees were constructed by the maximum likelihood method using unambiguously aligned nucleotide sites. The trees of rpoB and ITS2 are rooted on each midpoint. The bootstrap values (>50%) obtained from 1000 resamplings are given at the nodes. Sequences of the taxa with the DDBJ/EMBL/GenBank accession numbers in brackets were obtained from the database.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4920589&req=5

pone.0156587.g003: Phylogeny of the sexual and asexual lineages based on partial sequences of mitochondria (CO1; a), an intracellular symbiont (rpoB; b), and the nuclear (ITS2; c) genome.The trees were constructed by the maximum likelihood method using unambiguously aligned nucleotide sites. The trees of rpoB and ITS2 are rooted on each midpoint. The bootstrap values (>50%) obtained from 1000 resamplings are given at the nodes. Sequences of the taxa with the DDBJ/EMBL/GenBank accession numbers in brackets were obtained from the database.
Mentions: Six haplotypes were found based on the mitochondrial CO1 sequences (1449 bp). These haplotypes were clearly divided into two groups corresponding to the sexual lineage and the asexual lineage (Fig 3a). Among the haplotypes of the sexual lineage, haplotype A1 was predominant (87.5%). In the asexual lineage, haplotype P1 was similarly predominant both on Okinawa (87.5%) and Ishigaki (66.7%). Each haplotype represented a group that was the most closely related among the CO1 sequences of all mealybug species examined and clustered into clades with high bootstrap values (Fig 3a). A total of 35 nucleotide sites were substituted (2.4%; 16 transitions and 19 transversions involving eight amino acid substitutions) between haplotypes A1 and P1.

Bottom Line: Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a "cost of males." Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations.Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage.This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.

View Article: PubMed Central - PubMed

Affiliation: National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan.

ABSTRACT
Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a "cost of males." Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations. But the evolution of sexual reproduction remains unclear, because we have limited examples that demonstrate the relative success of sexual lineages in the face of competition from asexual lineages in the same environment. Here we investigated a sympatric occurrence of sexual and asexual reproduction in the pineapple mealybug, Dysmicoccus brevipes. This pest invaded southwestern Japan, including Okinawa and Ishigaki Islands, in the 1930s in association with imported pineapple plants. Our recent censuses demonstrated that on Okinawa sexually reproducing individuals can coexist with and even dominate asexual individuals in the presence of habitat and resource competition, which is considered to be severe for this nearly immobile insect. Molecular phylogeny based on partial DNA sequences in the mitochondrial and nuclear genomes, as well as the endosymbiotic bacterial genome, revealed that the asexual lineage diverged from a common sexual ancestor in the relatively recent past. In contrast, only the asexual lineage exhibiting obligate apomictic thelytoky was discovered on Ishigaki. Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage. Differences in biotic and/or abiotic selective forces operating on the two islands might be the cause of this discrepancy. This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.

No MeSH data available.


Related in: MedlinePlus