The effect of ploidy level on fitness in parthenogenetic flatworms

D’Souza, Thomas G.; Storhas, Martin; Michiels, Nico K.

doi:10.1111/j.1095-8312.2005.00482.x

Cited by 18 publications

(25 citation statements)

References 66 publications

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“…More is not inevitably better. In fact, higher ploidy may be harmful [50]. To determine if ploidy-level variation can affect disease spread and resistance evolution, we must first ask: Is increased ploidy associated with higher allelic diversity at resistance genes?…”

Section: Resultsmentioning

confidence: 99%

Is more better? Polyploidy and parasite resistance

2012

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Ploidy-level variation is common and can drastically affect organismal fitness. We focus on the potential consequences of this variation for parasite resistance. First, we elucidate connections between ploidy variation and key factors determining resistance, including allelic diversity, gene expression and physiological condition. We then argue that systems featuring both natural and artificially manipulated ploidy variation should be used to evaluate whether ploidy level influences host -parasite interactions.Keywords: polyploidy; host-parasite interactions; allelic diversity; gene expression; host condition 1. INTRODUCTION Polyploidization 1 has generated variation in ploidy level within and across species [1,2], and new examples are continually being discovered, particularly in animals [3]. Intraspecific ploidy-level variation is associated with a suite of connections between polyploidy and biological phenomena [4,5], and has the potential to influence fitness-related traits [6,7]. We discuss whether ploidy variation could mediate resistance to a ubiquitous enemy-parasites (defined here as an organism that harms its host). Although current theory suggests ploidy level can profoundly influence infection dynamics and host-parasite evolution [8,9], data are scarce [10,11]. PLOIDY AND IMMUNE FUNCTIONPolyploidy (i.e. autopolyploidy) could directly influence immune response to a parasite attack in at least two ways. Firstly, the addition of a new genome may increase allelic diversity. Higher allelic diversity at immune genes could help hosts recognize a greater diversity of parasites [12]. Secondly, if the additional genome copies are expressed, then polyploids may generate higher amounts of gene products related to immune function.(a) Allelic diversity and immune function The high allelic diversity of immune genes is partly a consequence of parasite-mediated selection for rare genotypes and/or novel immune functions [13]. Parasitemediated selection may generate such diversity through mechanisms such as heterozygote advantage [14] and negative frequency-dependence [13]. Heterozygote advantage could be influenced by ploidy level because the extra alleles present in polyploids may increase the probability of heterozygosity for an individual at a given locus. The presence of an extra genome could also increase the likelihood that an individual possesses a rare genotype at resistance loci; this would be advantageous if parasite-mediated negative frequency-dependent selection favours rare genotypes.Studies from natural populations have documented connections between parasite-mediated selection and the maintenance of allelic variation at genes associated with immune function [12,15]. Genetic polymorphism can play an important role in generating variation in recognition molecules [16], and diversity is important for disease resistance in host individuals and populations [17,18]. Furthermore, measures of genome-wide genetic variation (e.g. microsatellite heterozygosity [19,20]) are often correlated with individual immune ...

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Section: Resultsmentioning

confidence: 99%

Is more better? Polyploidy and parasite resistance

2012

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“…This ploidy cycle from triploidy to tetraploidy and back represents a two‐step form of sexual reproduction (Fig. 1C) and leads to stable ploidy frequencies, despite low fitness of tetraploids (D’Souza et al. , 2005).…”

Section: Methodsmentioning

confidence: 99%

Correlations between sex rate estimates and fitness across predominantly parthenogenetic flatworm populations

D’Souza

Michiels

2007

J of Evolutionary Biology

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One explanation for the success of sexual reproduction is that sex increases the efficacy of natural selection. Recombination and segregation lead to fitness variance among offspring which then offers a wider target for natural selection. Consequently, adaptation to changing environments is accelerated and population mean fitness will increase. We investigated whether low levels of sex are associated with increased fitness variance and mean in parthenogenetic biotypes of the planarian flatworm Schmidtea polychroa. Parthenogenetic S. polychroa are triploid and reproduce clonally with occasional sexual reproduction. By‐products and measures of occasional sex are the local presence of tetraploids and elevated levels of genotypic diversity. We correlated the proportion of tetraploids and genotypic diversity with fitness attributes of six genetically differentiated locations within one meta‐population. Results indicate strong, positive correlations with variance and with mean offspring number produced during a 5‐week period. The ecological and evolutionary implications for the maintenance of parthenogenetic S. polychroa are discussed.

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“…However, the sperm does not contribute genetically to offspring: Paternal alleles are expelled with one of the polar bodies or degenerate within the zygote, leading to clonal offspring (Benazzi Lentati, 1970). It has been shown that tetraploid individuals can only exist and be maintained through these sexual processes (D'Souza, Storhas & Michiels, 2005). In fact, tetraploids in this species are derived from triploids through such rare sexual events (D'Souza et al, 2004).…”

Section: Model Systemmentioning

confidence: 98%

“…For genetic analysis, two highly polymorphic trinucleotide microsatellites (SpATT12 and SpATT20), which were developed for and have been previously used in planarian genetic studies (see Pongratz et al, 2001Pongratz et al, , 2003Pongratz, Gerace & Michiels, 2002;D'Souza et al, 2004D'Souza et al, , 2005, were amplified using PCR (Buffer 1·, MgCl 2 2.5 mmol, dNTPs 0.2 mmol, primer 0.5 lmol, Taq polymerase 0.08 u) and sized on an ABI 3130xl Genetic Analyzer (Applied Biosystems, Foster City, CA, U.S.A.). For sizing, a master mix including 1170 lL deionised formamide and 30 lL Gene ScanÔ size standard (in this case ROX Ô ; Applied Biosystems) was prepared, and 12-lL aliquots were mixed with the corresponding amount of PCR product.…”

Section: Dna Extraction and Genotypingmentioning

confidence: 99%

“…Throughout this manuscript, the term 'clone' is defined as a group of individuals with the same ploidy and genotype irrespective of their descent. A theoretical model has shown that the coexistence of triploids and tetraploids is maintained through occasional sex (D'Souza et al, 2005). Independent metapopulations are located in Southern Germany (Ammersee, Chiemsee and Lake Constance) and Switzerland (Lake Sempach, Lake Hallwil and Lake Zü rich) and inhabited by purely parthenogenetic individuals.…”

Section: Statistical Analysesmentioning

confidence: 99%

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Population genetic structure of parthenogenetic flatworm populations with occasional sex

et al. 2012

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Summary 1. Sexual populations are expected to perform better in fluctuating environments than asexuals because recombination provides the potential to adapt to changing environments due to increased genetic variation. Nevertheless, some asexual species show comparably high levels of genotypic diversity. Such diversity might be achieved through gene flow between coexisting sexual and asexual populations or through sexual events within asexual populations. 2. Evidence for occasional sex in the flatworm Schmidtea polychroa was previously found at one specific site that is inhabited by parthenogenetic forms. There, varying rates of sex between subpopulations, reaching up to 12%, were observed. Past recurrent sexual processes left a significant genetic signature in the population genetic structure of this population. In the present study, we examined the population genetic structure of six independent metapopulations (lakes) of the freshwater planarian flatworm S. polychroa, to confirm the presence of occasional sex and that its population genetic consequences can be generalised. 3. Using microsatellites, we found varying rates of occasional sex among subpopulations. Metapopulations showed medium to high levels of genotypic diversity that correlated with the rate of sex. 4. We conclude that occasional sex has considerable consequences for population genetic structure of parthenogenetic species and promotes diversity that might allow response to the particular type of selection that is usually predicted to favour sexual reproduction. This reproductive strategy provides genetic characteristics required for selection to act on, and might, therefore, explain the success of this parthenogenetic species.

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The effect of ploidy level on fitness in parthenogenetic flatworms

Cited by 18 publications

References 66 publications

Is more better? Polyploidy and parasite resistance

Is more better? Polyploidy and parasite resistance

Correlations between sex rate estimates and fitness across predominantly parthenogenetic flatworm populations

Population genetic structure of parthenogenetic flatworm populations with occasional sex

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