Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails

Krois, Nicole R.; Cherukuri, Anvesh; Puttagunta, Nikhil; Neiman, Maurine

doi:10.1098/rsbl.2013.0422

“…2009) and tissue regeneration rate (Krois et al. 2013) of asexual versus sexual P. antipodarum . Together, these results hint that asexual P. antipodarum may realize tissue‐ and individual‐level growth advantages connected to higher per‐organism gene expression levels (Neiman et al.…”

Section: Discussionmentioning

confidence: 99%

“…Another potential non-mutually exclusive explanation for why sexual P. antipodarum grow and mature more slowly than their asexual counterparts is provided by the higher per-unit mass RNA content (Neiman et al 2009) and tissue regeneration rate (Krois et al 2013) of asexual versus sexual P. antipodarum. Together, these results hint that asexual P. antipodarum may realize tissue-and individual-level growth advantages connected to higher perorganism gene expression levels (Neiman et al 2013b).…”

Section: Discussionmentioning

confidence: 99%

Effects of polyploidy and reproductive mode on life history trait expression

Larkin

¹

,

Tucci

²

,

Neiman

³

2016

Ecology and Evolution

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Ploidy elevation is increasingly recognized as a common and important source of genomic variation. Even so, the consequences and biological significance of polyploidy remain unclear, especially in animals. Here, our goal was to identify potential life history costs and benefits of polyploidy by conducting a large multiyear common garden experiment in Potamopyrgus antipodarum, a New Zealand freshwater snail that is a model system for the study of ploidy variation, sexual reproduction, host–parasite coevolution, and invasion ecology. Sexual diploid and asexual triploid and tetraploid P. antipodarum frequently coexist, allowing for powerful direct comparisons across ploidy levels and reproductive modes. Asexual reproduction and polyploidy are very often associated in animals, allowing us to also use these comparisons to address the maintenance of sex, itself one of the most important unresolved questions in evolutionary biology. Our study revealed that sexual diploid P. antipodarum grow and mature substantially more slowly than their asexual polyploid counterparts. We detected a strong negative correlation between the rate of growth and age at reproductive maturity, suggesting that the relatively early maturation of asexual polyploid P. antipodarum is driven by relatively rapid growth. The absence of evidence for life history differences between triploid and tetraploid asexuals indicates that ploidy elevation is unlikely to underlie the differences in trait values that we detected between sexual and asexual snails. Finally, we found that sexual P. antipodarum did not experience discernable phenotypic variance‐related benefits of sex and were more likely to die before achieving reproductive maturity than the asexuals. Taken together, these results suggest that under benign conditions, polyploidy does not impose obvious life history costs in P. antipodarum and that sexual P. antipodarum persist despite substantial life history disadvantages relative to their asexual counterparts.

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“…Endopolyploidy is also involved in wound healing in Drosophila melanogaster, where polyploidy and cell fusion were shown to be directly important in repairing damaged epithelium at wound sites (Losick et al 2013). This effect may also translate to whole-organism polyploids: A tetraploid morph of a New Zealand snail has faster wound repair than its diploid counterpart, although whether this arises directly from its polyploid state rather than an associated effect remains to be seen (Krois et al 2013).…”

Section: Big Cells and Rapid Growth-developmental Roles Of Somatic Pomentioning

confidence: 99%

Genome management and mismanagement—cell-level opportunities and challenges of whole-genome duplication

Yant

¹

,

Bomblies

²

2015

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Whole-genome duplication (WGD) doubles the DNA content in the nucleus and leads to polyploidy. In whole-organism polyploids, WGD has been implicated in adaptability and the evolution of increased genome complexity, but polyploidy can also arise in somatic cells of otherwise diploid plants and animals, where it plays important roles in development and likely environmental responses. As with whole organisms, WGD can also promote adaptability and diversity in proliferating cell lineages, although whether WGD is beneficial is clearly context-dependent. WGD is also sometimes associated with aging and disease and may be a facilitator of dangerous genetic and karyotypic diversity in tumorigenesis. Scaling changes can affect cell physiology, but problems associated with WGD in large part seem to arise from problems with chromosome segregation in polyploid cells. Here we discuss both the adaptive potential and problems associated with WGD, focusing primarily on cellular effects. We see value in recognizing polyploidy as a key player in generating diversity in development and cell lineage evolution, with intriguing parallels across kingdoms.

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“…Another potential non-mutually exclusive explanation for why sexual P. antipodarum grow and mature more slowly than their asexual counterparts may be provided by the higher perunit mass RNA content (Neiman et al 2009) and tissue regeneration rate (Krois et al 2013) of asexual vs. sexual P. antipodarum. Both of these results suggest that asexual P. antipodarum may realize tissue-and individual-level growth advantages connected to higher per-organism gene expression levels (Neiman et al 2013a).…”

Section: Effects Of Reproductive Mode Ploidy Level and Founder Sourmentioning

confidence: 99%

Effects of polyploidy and reproductive mode on life history trait expression

Larkin¹

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Ploidy elevation is increasingly recognized as a common and important source of genomic variation. Even so, the consequences and biological significance of polyploidy remain unclear, especially in animals. Here, our goal was to identify potential life history costs and benefits of polyploidy by conducting a large multiyear common garden experiment in Potamopyrgus antipodarum, a New Zealand freshwater snail that is a model system for the study of ploidy variation, sexual reproduction, host–parasite coevolution, and invasion ecology. Sexual diploid and asexual triploid and tetraploid P. antipodarum frequently coexist, allowing for powerful direct comparisons across ploidy levels and reproductive modes. Asexual reproduction and polyploidy are very often associated in animals, allowing us to also use these comparisons to address the maintenance of sex, itself one of the most important unresolved questions in evolutionary biology. Our study revealed that sexual diploid P. antipodarum grow and mature substantially more slowly than their asexual polyploid counterparts. We detected a strong negative correlation between the rate of growth and age at reproductive maturity, suggesting that the relatively early maturation of asexual polyploid P. antipodarum is driven by relatively rapid growth. The absence of evidence for life history differences between triploid and tetraploid asexuals indicates that ploidy elevation is unlikely to underlie the differences in trait values that we detected between sexual and asexual snails. Finally, we found that sexual P. antipodarum did not experience discernable phenotypic variance‐related benefits of sex and were more likely to die before achieving reproductive maturity than the asexuals. Taken together, these results suggest that under benign conditions, polyploidy does not impose obvious life history costs in P. antipodarum and that sexual P. antipodarum persist despite substantial life history disadvantages relative to their asexual counterparts.

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Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails

Cited by 22 publications

References 23 publications

Effects of polyploidy and reproductive mode on life history trait expression

Effects of polyploidy and reproductive mode on life history trait expression

Genome management and mismanagement—cell-level opportunities and challenges of whole-genome duplication

Effects of polyploidy and reproductive mode on life history trait expression

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