Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations

BACKGROUND: Models of the maintenance of sex predict that one reproductive strategy, sexual or parthenogenetic, should outcompete the other. Distribution patterns may reflect the outcome of this competition as well as the effect of chance and historical events. We review the distribution data of sexual and parthenogenetic biotypes of the planarian Schmidtea polychroa. RESULTS: S. polychroa lives in allopatry or sympatry across Europe except for Central and North-Western Europe, where sexual individuals have never been reported. A phylogenetic relationship between 36 populations based on a 385 bp fragment of the mitochondrial cytochrome oxidase I gene revealed that haplotypes were often similar over large geographic distances. In North Italian lakes, however, diversity was extreme, with sequence differences of up to 5% within the same lake in both sexuals and parthenogens. Mixed populations showed "endemic" parthenogenetic lineages that presumably originated from coexisting sexuals, and distantly related ones that probably result from colonization by parthenogens independent from sexuals. CONCLUSIONS: Parthenogens originated repeatedly from sexuals, mainly in Italy, but the same may apply to other Mediterranean regions (Spain, Greece). The degree of divergence between populations suggests that S. polychroa survived the ice ages in separate ice-free areas in Central, Eastern and Southern Europe and re-colonised Europe after the retreat of the major glaciers. Combining these results with those based on nuclear markers, the data suggest that repeated hybridisation between sexuals and parthenogenetic lineages in mixed populations maintains high levels of genetic diversity in parthenogens. This can explain why parthenogens persist in populations that were originally sexual. Exclusive parthenogenesis in central and western populations suggests better colonisation capacity, possibly because of inbreeding costs as well as hybridisation of sexuals with parthenogens

Protist-Type Lysozymes of the Nematode Caenorhabditis elegans Contribute to Resistance against Pathogenic Bacillus thuringiensis

Pathogens represent a universal threat to other living organisms. Most organisms express antimicrobial proteins and peptides, such as lysozymes, as a protection against these challenges. The nematode Caenorhabditis elegans harbours 15 phylogenetically diverse lysozyme genes, belonging to two distinct types, the protist- or Entamoeba-type (lys genes) and the invertebrate-type (ilys genes) lysozymes. In the present study we characterized the role of several protist-type lysozyme genes in defence against a nematocidal strain of the Gram-positive bacterium Bacillus thuringiensis. Based on microarray and subsequent qRT-PCR gene expression analysis, we identified protist-type lysozyme genes as one of the differentially transcribed gene classes after infection. A functional genetic analysis was performed for three of these genes, each belonging to a distinct evolutionary lineage within the protist-type lysozymes (lys-2, lys-5, and lys-7). Their knock-out led to decreased pathogen resistance in all three cases, while an increase in resistance was observed when two out of three tested genes were overexpressed in transgenic lines (lys-5, lys-7, but not lys-2). We conclude that the lysozyme genes lys-5, lys-7, and possibly lys-2 contribute to resistance against B. thuringiensis, thus highlighting the particular role of lysozymes in the nematode's defence against pathogens

Reproductive modes, ploidy distribution, and supernumerary chromosome frequencies of the flatworm Polycelis nigra (Platyhelminthes: Tricladida)

The hermaphroditic flatworm, Polycelis nigra, is characterized by two reproductive biotypes which differ with respect to ploidy; sexual individuals are diploid (n = 8, 2× = 16) and pseudogamous parthenogenetic individuals are polyploid (typically 3×). We have collected and karyotyped individuals from 15 sampling sites (13 in mid to northern Italy, one in Great Britain and one in The Netherlands). We found that biotypes can exist alone or in sympatry, and identified purely diploid, mixed diploid-polyploid, and purely polyploid populations. Karyotype data show that in addition to the normal autosome complement, B chromosomes of differing morphology as well as stable aneuploid chromosomes (extra-A) were found almost exclusively in polyploids (11 of 12 sites). We extensively sampled Lago di Toblino (northern Italy), a pure polyploid population characterized by a submetacentric to metacentric, mitotically stable B chromosome, as well as a stable extra-A chromosome. Here, individuals having 1–3 B chromosomes were more abundant (61%) than those having no B’s, implying that B chromosome infection has little detrimental effect when occurring in low numbers. Furthermore, 66% of individuals from this population possessed extra-A chromosomes, although it is unclear whether these elements are aneuploid autosomes or B chromosomes of different morphology. The ubiquity of these chromosomes, within asexuals in particular, is suggestive of a correlation between the origination of the elements and the evolution of polyploidy, or may reflect increased tolerance of parthenogenetic genomes to aneuploidy.

Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations

Background: Models of the maintenance of sex predict that one reproductive strategy, sexual or parthenogenetic, should outcompete the other. Distribution patterns may reflect the outcome of this competition as well as the effect of chance and historical events. We review the distribution data of sexual and parthenogenetic biotypes of the planarian Schmidtea polychroa. Results: S. polychroa lives in allopatry or sympatry across Europe except for Central and North-Western Europe, where sexual individuals have never been reported. A phylogenetic relationship between 36 populations based on a 385 bp fragment of the mitochondrial cytochrome oxidase I gene revealed that haplotypes were often similar over large geographic distances. In North Italian lakes, however, diversity was extreme, with sequence differences of up to 5% within the same lake in both sexuals and parthenogens. Mixed populations showed "endemic" parthenogenetic lineages that presumably originated from coexisting sexuals, and distantly related ones that probably result from colonization by parthenogens independent from sexuals. Conclusions: Parthenogens originated repeatedly from sexuals, mainly in Italy, but the same may apply to other Mediterranean regions (Spain, Greece). The degree of divergence between populations suggests that S. polychroa survived the ice ages in separate ice-free areas in Central, Eastern and Southern Europe and re-colonised Europe after the retreat of the major glaciers. Combining these results with those based on nuclear markers, the data suggest that repeated hybridisation between sexuals and parthenogenetic lineages in mixed populations maintains high levels of genetic diversity in parthenogens. This can explain why parthenogens persist in populations that were originally sexual. Exclusive parthenogenesis in central and western populations suggests better colonisation capacity, possibly because of inbreeding costs as wel

Reduced Male Allocation in the Parthenogenetic Hermaphrodite Dugesia polychroa

Parthenogenetic lineages that arise in a hermaphroditic, sexual population will inherit the male function from their sexual progenitors. Natural selection then acts to reduce male allocation of the parthenogens, freeing resources presumably for the female function. Depending on age and the available genetic variation, one therefore expects to find reduced male allocation in naturally occurring parthenogenetic lineages. We investigated the allocation to sperm production in the hermaphroditic flatworm Dugesia polychroa in three lakes containing a sexual (S), a (pseudogamous) parthenogenetic (P), and a mixed sexual-parthenogenetic population (M). Parthenogenetic lineages from M were assumed to be relatively young due to recurrent origins from the coexisting sexuals, whereas those from P were assumed to be older on biogeographical grounds. As predicted, we found drastically reduced sperm production in parthenogens compared to sexuals, even in the parthenogenetic lineages from M, which may be younger. M parthenogens did not have more testes, but produced more sperm than individuals from the purely parthenogenetic population (P). However, the latter result could not be reproduced with laboratory-raised animals and therefore may be a consequence of different ecological conditions in the different lakes, for example, differences in mating rates. To study the behavioral component of male allocation, copulation frequencies were recorded for sexuals from M and for parthenogens from P. Compared to the drastic reduction in sperm production, copulation frequency was less reduced in parthenogens. This may be a consequence of allosperm limitation in pseudogamous parthenogenetic populations.

Spatial and ecological overlap between coexisting sexual and parthenogenetic Schmidtea polychroa (Tricladida; Platyhelminthes)

Theoretical models on the costs and benefits of sexual reproduction usually assume that sexual and parthenogenetic individuals coexist and are identical, except for their mode of reproduction. Empirical studies, however, show that conspecific sexuals and parthenogens can differ in ecological preferences and geographical distribution, which complicates the investigation of the costs and benefits of sex. The freshwater planarian Schmidtea polychroa exists in a sexual and a sperm-dependent, parthenogenetic form. The latter produce fertile sperm and mate, but received sperm is used only to induce parthenogenetic embryo development. We compared the spatial and ecological distribution between forms within a lake from which both had been reported. Forty samples showed large differences in the relative frequencies of sexuals and parthenogens. Nineteen samples contained both biotypes. All but one of the 13 ecological parameters that we measured, could not explain a significant part of the variance in relative abundance of each type. Only leech abundance had a significant, negative effect on the presence of sexual individuals. The causes of this effect remained unclear. We also estimated the amount of genetic isolation between sites and between reproductive modes, using body coloration as a genetic marker. Large differences were found between sites, suggesting isolation of local populations by migration barriers. There were smaller differences between sexuals and parthenogens within sites, suggesting that genetic exchange between biotypes may be limited. We conclude that there appears to be weak niche differentiation between sexuals and parthenogens in Lago di Caldonazzo in late summer. Fluctuations in relative frequency appears to be a consequence of low dispersal between local populations and stochastic effects within them.

Occasional sex in an 'asexual' polyploid hermaphrodite.

Asexual populations are usually considered evolutionary dead-ends because they lack the mechanisms to generate and maintain sufficient genetic diversity. Yet, some asexual forms are remarkably widespread and genetically diverse. This raises the question whether asexual systems are always truly clonal or whether they have cryptic forms of sexuality that enhance their viability. In the planarian flatworm Schmidtea polychroa parthenogens are functional hermaphrodites (as are their sexual conspecifics), copulate and exchange sperm. Sperm is required for initiation of embryogenesis but usually does not contribute genetically to the offspring (sperm-dependent parthenogenesis). Using karyology and genotyping of parents and offspring, we show that in a purely parthenogenetic population an estimated 12% of all offspring are the result of partial genetic exchange. Several processes of chromosome addition and loss are involved. Some of these result in an alternation between a common triploid and a rare tetraploid state. We conclude that genetic recombination does not necessarily require segregation and fusion within the same generation, as is the case in most sexual species. These occasional sexual processes help to explain the geographical dominance of parthenogens in our study species