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Abstract

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

Asexual forms of invertebrates are relatively common. They are often more successful than their sexual progenitors. Especially in insects, the pattern called geographical parthenogenesis shows that asexuality is important in speciation and ecological adaptation. In geographical parthenogenesis the clones have a wider distribution than the sexual forms they originate from. This indicates that they have a broader niche they may utilize successfully. The cause of this apparent success is, however, hard to come by as the term asexuality covers separate phenomena that are hard to disentangle from the mode of reproduction itself. Asexual insects are often polyploid, of hybrid origin, or both and these phenomena have been argued to explain the distribution patterns better than clonality. In this study we survey the literature on arthropods with geographical parthenogenesis in an attempt to clarify what evidence there is for the different phenomena explaining the success of the clonal forms. We focus on the few species where knowledge of distribution of different ploidy levels allows for a distinction of contributions from different phenomena to be made. Our survey support that asexuality is not the only factor underlying the success of all asexuals. Evidence about the importance of a hybrid origin of the clones is found to be meagre as the origin of clones is unknown in the majority of cases. Asexuality, hybridity and polyploidy are intertwined phenomena that each and all may contribute to the success of clonal taxa. Polyploidy, however, emerges as the most parsimonious factor explaining the success of these asexual invertebrate taxa.

Sexual reproduction, Mendelian genetics and diploidy are intertwined phenomena. Each can be argued to be a major invention in the history of life. Nevertheless, a number of eukaryotes have reverted to obligate asexuality.

Among taxa with both sexual and obligate clonal forms (that may or may not have a nominal species status) the distribution pattern termed geographical parthenogenesis (Vandel 1928) is common. In geographical parthenogenesis (GP) the sexual forms have a central, or limited, distribution while the clonal forms most often surround the central area or are found towards e.g. higher altitudes or latitudes. In a majority of the cases the clones also have a much wider distribution and ecological tolerance than the sexual forms they originate from (Beaton and Hebert 1988; Parker and Niklasson 2000; Schön et al. 2000; Stenberg et al. 2003). This spatial distribution of clones has been attributed to reproductive mode, elevated ploidy level or hybrid origin (Kearney 2005) or all of these. Lundmark (2006) pointed out that they are separate phenomena. In the following we shall try to disentangle them from each other and use insects with their immense biological diversity to support the argumentation.

We take asexual reproduction first. Given that all other things are equal, asexuality gives an automatic twofold reproductive advantage over sexual reproduction (MaynardSmith 1978). Yet sexual reproduction prevails among animals and plants; asexual taxa are seen to be evolutionarily inferior, and often short-lived (White 1970; Bell 1982). On the other hand, many asexuals are extremely successful so that many are pests (Stenberg and Lundmark 2004) and some are certainly long-lived and speciose taxa (Mark Welch and Meselson 2000). On the plus side, the asexuals can reproduce rapidly. They are efficient colonizers as a single female may start a new population. On the minus side they lack genetic recombination (Felsenstein 1974; Lokki 1976a; Barton and Charlesworth 1998); if they have it, they in general have mechanisms that result in genetic erosion and enforce homozygosity (Suomalainen et al. 1987). Bachtrog (2003) observed the rates of incorporation of beneficial mutations within parts of the same genome that were subject to recombination and accumulation of detrimental ones in non-recombining parts (neo-Y) in Drosophila miranda. She found out that deleterious mutations accumulate in the non-recombining part of the genome, while there is evidence for rapid adaptive evolution in the recombining part. Accordingly, there is both theoretical and experimental evidence for the importance of genetic recombination in evolution.

All asexual (apomictic) angiosperms are polyploid (Asker and Jerling 1992) but not all polyploid plants are asexual. In the Animal Kingdom, polyploidy is mainly restricted to asexual taxa but there are many diploid asexuals as well (Suomalainen et al. 1987). The incidence of plant and animal polyploids has, in general, seen to be correlated with increasing geographic latitude so that areas which were ice covered during the Pleistocene glaciations harbour a high frequency of polyploids (Stebbins 1950; Seiler 1961). Stebbins (1984) argued that polyploid frequency is correlated with the degree of glaciation rather than latitude. Brochmann et al. (2004) found, in a survey of the circumarctic flora that there is no good correlation with the degree of glaciation. In the course of repeated glacial cycles, the distributions of animals and plants expand and contract (Kearney 2005), with the result that inbreeding and drift depress the genetic diversity (Hewitt 1996; Pamilo and Savolainen 1999). Gradual, even rates of speciation are disturbed and the proportion of abrupt speciation events, mainly through polyploid formation, increases (Dynesius and Jansson 2000).

Polyploid formation is in general seen to involve hybridization between two species (allopolyploidy), while the alternative, autopolyploidy, (where the multiple chromosomes come essentially from the same genome) is thought to be rare or non-existent (Stebbins 1950).

Several cases of verified autopolyploids have, however, been found among animals (Seiler 1963) and plants (Soltis and Soltis 1993, 2000; Van Dijk and Bakx-Schotman 1997; Borgen and Hultgård 2003; Yamane et al. 2003). On the other hand, the difference between allo- and allopolyploids need not be sharp; it is more or less a question of how far apart genetically the involved taxa are from each other. Polyploidy gives, at least theoretically, a new lease of life to asexuals faced with a steady accumulation of deleterious mutations (Lokki 1976b). Furthermore, polyploids show stronger heterosis effects than corresponding diploid hybrids (Comai 2005).

Already Linnaeus (1774) saw in “Systema Vegetabilium” hybridization as a major factor giving rise to new species of plants, a point emphasized by students of plant evolution ever since (Arnold 1997). Crosses between different lineages are, however, often poorly viable (Arnold 1997; Ramsey and Schemske 2002). Reductions in hybrid fitness may be a consequence of several factors separately or in combination (Rhode and Cruzan 2005). On the other hand, hybrids can have superior fitness because of heterosis (Lerner 1954; Lynch 1991; Burke and Arnold 2001). Clonal reproduction saves a fit hybrid genotype from meiotic disturbances and hybrid breakdown (Coyne and Orr 1998; Orr and Turelli 2001), a circumstance that is of paramount importance for polyploids (Comai 2005). Students of asexuality highlight, in general, the positive contribution of hybridity in the evolution of asexual animals (Kearney 2005). Cloning may freeze the permanent state of heterozygosity and heterosis effects; something that could be adaptively beneficial in new or marginal habitats (Kearney 2005).

Stebbins (1950) emphasized the importance of asexuality: the mode of reproduction and the stationary clonal genome as an explanation for GP. The clonal forms fail to compete with the sexuals in the central area, but have a superior ability to colonize new habitats. In pristine areas asexuals may also benefit from the ability to reproduce rapidly and take advantage of resources, making subsequent immigration by sexual forms harder (reviewed by Parker and Niklasson 2000). This, however, is based on the assumption that the diploid sexual forms actually are able to utilize the areas in question.

A polyploidisation of the genome on the other hand may result in unique gene combinations and altered expression patterns, enlarged body, or cell size and elevated level of heterozygosity (Parker and Niklasson 2000). This has been argued to make polyploid clones more tolerant to abiotic stress (e.g. temperature, desiccation or salinity) and they have, consequently, wider ecological tolerances in what environments and habitats they may utilize in comparison with their sexual ancestors (Lewis 1980).

What complicates the picture is that most animals with GP only have diploid sexuals and a single ploidy level of parthenogens (typically triploids); the clones may also be of either allo- or autopolyploid origin (i.e. hybrids or not). As these different phenomena often are linked, it is difficult to deduce what is actually responsible for the apparent success of clonal forms in GP taxa. Laboratory corroboration has proven inconclusive and hard to come by (Wetherington et al. 1987; Zhang and Lefcort 1991; Gade and E. D. Parker 1997) because of the nature of clonal samples. All clonal lineages need not be more successful than sexuals (because of polyploidy or hybrid vigour), it suffices that a few or a single one are. Selection strongly furthers the few that manage to overcome the problems associated with genome duplication and hybrid dysfunction. Because of that, it is of little value to state that e.g. synthesised triploid lineages as a group are worse than diploid sexual relatives with regard to a life history trait. Different clonal lineages of the same ploidy level do not make up a true population as they are reproductively isolated from each other, and population means of a trait are thus inapplicable. As long as any polyploid lineage shows a higher fitness in laboratory tests, the study can instead be considered supporting a potential superiority of the clones.

To distinguish the effect of the different phenomena on ecological and geographical success of different forms, one needs to study taxa of both hybrid and non-hybrid origin where variation in breeding system and ploidy level are separate. Further, it is important to avoid taxa where other factors directly affect distributions of one form e.g. internal parasites, or pseudogamous asexuals. Even though pseudogamous taxa are asexual as the male genome does not get incorporated in the genome of the offspring, sperm are needed to trigger off the development of eggs. Accordingly, the distribution pattern of a pseudogamous taxon is tied to the distribution of the sexual taxon.

We survey here the literature published on invertebrate taxa with geographical parthenogenesis in an attempt to evaluate the support for asexuality per se, hybridity or polyploidy explaining these patterns. We also elaborate on the few cases with several degrees of ploidy where the distributions of different ploidy forms are well known. We do not try to characterize ecological conditions or habitats where clones are superior, and just accept that they have some attributes the sexual forms lack which allow these asexuals to have a more extensive distribution.

Arthropod taxa with geographical parthenogenesis

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

For reasons stated above we chose to limit the following survey to taxa with clones that reproduce through obligate parthenogenesis. We only included taxa that have chromosomal sex determination and where ploidy level has been verified in both the sexual and the clonal forms. We excluded internal parasites and taxa with sperm dependent asexuals. Taken together, when surveying every reported case of arthropods with GP fulfilling our criteria, we found support for 35 known cases (Table 1). As a single case, or complex, we count a sexual ancestor and its clonal descendants, no matter if the different forms have nominal species status or not, as taxonomical status are not of relevant interest to the survey. 20 out of these 35 taxa have a single polyploid clonal form, three have only diploid clones and 12 taxa have asexual forms with more than one ploidy level (Table 1).

Table 1.  Arthropods with geographical parthenogenesis or geographical polyploidy. An outline of invertebrate animals with geographical parthenogenesis, or geographical polyploidy, and obligate asexual forms where ploidy levels are known. Internal parasites and pseudogamous species are excluded. Hybrid or non-hybrid origin of clones is noted in cases where it is known. Many references are cited through Suomalainen et al. (1987).
Taxa with GP and more than one ploidy level or geographical polyploidy
LepidopteraDahlica triquetrella, sexual 2n, clonal 2 and 4n,non-hybridSuomalainen 1969, this study
CladoceraDaphnia pulex, sexual 2n, clonal 2, 4n, hybridBeaton and Hebert 1988; Adamowicz et al. 2002
OstracodaHeterocypris, sexual glaucus 2n, clonal incongruens 2, 3, 4n, hybridChaplin 1992; Turgeon and Hebert 1994, 1995; Butlin et al. 1998
 Cypricercus reticulatus, sexual 2n, clonal 2, 3n, hybridHoff 1942; Turgeon and Hebert 1994, 1995; Butlin et al. 1998
 Eucypris virens, sexual 2n, clonal 2, 3n, hybridHorne and Martens 1999; Schön et al. 2000
PhasmatodeaBacillus, grandii sexual 2n, atticus clonal 2, 3nScali et al. 2003
AnostracaArtemia, sexual tunisiana 2n, clonal parthenogenetica 2, 3, 4nBrowne and Salle 1984; Suomalainen et al. 1987; Zhang and Lefcourt 1991; Lecher et al. 1995
BlattopteraPycnoscelus, sexual indicus 2n, clonal surinamensis 2, 3nRoth 1967; Parker and Niklasson 1995; Gade and Parker 1997
ColeopteraOtiorhychus scaber, sexual 2n, clonal 2, 3, 4nSuomalainen et al. 1987; Stenberg et al. 2003
 Otiorhychus chrysocomus, sexual 2n, clonal 3, 4nSuomalainen et al. 1987
 Barynotus moerens, sexual 2n, clonal 3, 5nSuomalainen et al. 1987
 Simo hirticornis, sexual 2n, clonal 3, 4nSuomalainen et al. 1987; Palm 1996
  
Species with GP and a single polyploid clonal form
IsopodaTrichoniscus, sexual: elisabethae 2n, clonal: coelebs 3nVandel 1940; Suomalainen et al. 1987
 Trichoniscus pusillus, sexual 2n, clonal 3n, hybridChristensen 1983
OrthopteraSaga pedo, sexual 2n, clonal 4nMatthey 1941; Suomalainen et al. 1987
DipteraProsimulium ursinum, sexual 2n, clonal 3nRothfels 1979
AcarinaHaemaphysalis longicornis, sexual 2n, clonal 3nHoogstral et al. 1968; Suomalainen et al. 1987
ColeopteraOtiorhychus, sexual squamosus 2n, clonal salicis 3nSuomalainen et al. 1987
 Otiorhychus sexual hormuzachii 2n, clonal ligustici 3nSuomalainen et al. 1987; Palm 1996
 Otiorhychus singularis, sexual 2n, clonal 3nSuomalainen et al. 1987
 Otiorhychus nodosus, sexual 2n, clonal 3nSuomalainen et al. 1987
 Polydrosus mollis, sexual 2n, clonal 2, 3nSuomalainen et al. 1987
 Liophleus tessulatus, sexual 2n, clonal 3nSuomalainen et al. 1987
 Bromius obscurus, sexual 2n, clonal 3nSuomalainen et al. 1987
 Barynotus squamosus, sexual 2n, clonal 3nSuomalainen et al. 1987
 Barynotus obscurus, sexual 2n, clonal 4nSuomalainen et al. 1987; Palm 1996
 Trachyphloeusaristatus, sexual 2n, clonal 3nSuomalainen et al. 1987; Palm 1996
 Trachyphloeus bifoveolatus, sexual 2n, clonal 3nSuomalainen et al. 1987; Palm 1996
 Trachyphloeus aristatus, sexual 2n, clonal 3nSuomalainen et al. 1987; Palm 1996
 Tropiphorus sexual alophoides 2n, clonal carinatus 3nSuomalainen et al. 1987; Palm 1996
 Tropiphorus terricola, sexual 2n, clonal 4nSuomalainen et al. 1987; Palm 1996
LepidopteraDahlica sexual fumosella 2n, clonal lichenella 4nSuomalainen et al. 1987
  
Species with GP and only diploid forms
BlattopteraPhyllodromica subaptera, sexual and clonal 2nKnebelsberger and Bohn 2003
DiplopodaNemasoma varicorne, sexual and clonal 2nEnghoff 1976a, 1976b; Jensen et al. 2002
OrthopteraWarramaba virgo, sexual 2n, clonal 2n, hybridWhite 1980

Three cases, Phyllodromica subaptera, Nemasoma varicorne and Warramba virgo, have only diploid clones and are, accordingly, cases of geographical parthenogenesis where polyploidy may be excluded as a factor contributing to the success of the asexuals. These taxa indicate that asexual reproduction may suffice to explain the distribution patterns. However, the hybrid origins of W. virgo are well known (Hewitt 1975; White 1980). As for N. varicorne, the ploidy level of clonal forms has only been determined in two specimens from the central area of distribution (Enghoff 1976a,b; Jensen et al. 2002), which is too few to rule out the existence of polyploid forms. Also in N. varicorne hybrid events may well be involved in the origin of the asexuals (Jensen et al. 2002), which, if true, negates the straightforward argument for parthenogenesis being the main reason behind the success of the clones.

In P. subaptera the ploidy levels from multiple specimens of several different samples of asexuals are known (Knebelsberger and Bohn 2003) and no polyploids have been found. In fact, the asexual forms all have a reduced chromosome number due to centric fusion of acrocentric chromosomes, something they share with some populations of sexual diploids. The geographical distributions of the different forms are well known. Sexual idividuals of P. subaptera are limited to the Iberian peninsula and some scattered populations in Portugal while the clones inhabit most of the Mediterranean countries and islands, Switzerland, and some of the Adriatic islands (Knebelsberger and Bohn 2003). This complex may well be the strongest evidence that asexuality alone may suffice to explain GP in invertebrate animals.

From the 20 taxa with GP and a single asexual form that also is polyploid the link between the two phenomena makes direct deductions hard. An argument can however be made that if polyploidy were not important in these taxa one ought to have recorded diploid clones, given that they exist at all in these taxa. An absence of diploid clones (or inability to distinguish them from the sexual females in the central areas of distribution) does not contradict that polyploidy is important for geographical success in these cases. The fact that most examined cases of GP only have polyploid clones, however, may be interpreted as support for that hypothesis. Effects of a hybrid origin should of course be considered but only a single one, Trichoniscus pusillus, is reported to be of hybrid origin (Christensen 1983). In the majority of cases the origins of the asexuals are simply not studied in sufficient detail.

Among the 12 taxa with clonal forms of multiple ploidy levels Otiorhynchus scaber and Dahlica (Solenobia) triquetrella are the cases that most clearly conform to geographical polyploidy (Stenberg et al. 2003), where a higher ploidy level is linked with a wider distribution. In many others (e.g. Daphnia pulex) the trend of wider distribution with higher ploidy level is strong but often the distributions of different ploidy levels are not well known. Four of the 12 are known hybrids (Table 1) but also in this group the processes behind the origins of the asexuals are mostly unknown. Polydrusus mollis, on the other hand, clearly stands out as an exception in this group. The diploid sexuals of P. mollis have a relictual distribution and around them, in central Europe, triploid clones are found, while the diploid clones have spread further reaching eastern and northern Europe (Lokki et al. 1976). However, P. mollis is the only clonal weevil that can fly, and allozyme analysis indicates that the asexuals probably are monophyletic (Suomalainen et al. 1987). In the other cases with multiple clonal forms a polyphyletic origin of asexuals appears to be the norm.

The weevil genus Otiorhynchus has hundreds of described species and quite a few have both sexual and clonal forms e.g. O. lepidopterus, O. nodosus, O. proximus, O. scaber and O. singularis (Jahn 1941; Suomalainen et al. 1987) and GP. A closer inspection of the distribution has, however, shown that in many species the sexual and clonal weevils are sympatric in the central areas of distribution (Stenberg et al. 2000, 2003).

Within the O. scaber complex there are four different forms, diploid sexuals and diploid, triploid and tetraploid parthenogens (Stenberg et al. 2003). The clones reproduce through apomixis (Suomalainen 1940), i.e. the development of eggs involves mitosis instead of meiosis, and the offspring are genetic copies of their mother. The extent of the area of distribution occupied by each ploidy level is positively correlated with the degree of polyploidy, and where distributions overlap there is sympatry (Fig. 1). As mentioned above, we (Stenberg et al. 2003) have introduced the term “geographical polyploidy” for such a pattern. Clonal lineages are polyphyletic and may well be of hybrid origin (Stenberg and Lundmark 2004). Clonal diversity is high in central populations and decreases towards the margins (Stenberg et al. 2003). Multiple colonization events are needed to explain the present distribution in marginal areas and a number of clonal lineages are found within the outer fringes of distribution, of each of the three different ploidy levels (Stenberg et al. 2003). The important point is that asexuality does not explain the stepwise increase in distribution between different ploidy levels. What we observe is the spread over Europe following the latest glaciation. The different forms of O. scaber have overwintered the Ice Ages within well-known refugial areas that also have sheltered many other animals and plants (Stenberg et al. 2000). The diploids, both clones and sexuals, have not been able to spread from these refugia even though diploid clones should have the same benefits as polyploid clones concerning dispersal ability. The degree of ploidy, and not the mode of reproduction, is the main factor that explains the present distribution of O. scaber clones. A hybridization event that led to polyploidy can, of course, have also given increased heterosis effects.

image

Figure 1. Distribution of different ploidy levels in Otiorhynchus scaber. Diploid sexuals and all clonal forms are sympatric in two small areas in the eastern Alps in Austria and Slovenia (black dots). Triploid and tetraploid clones inhabit most of the central European montane and submontane areas (dark grey shading), and tetraploids alone populate almost every native spruce forest of Europe (light grey shading) (Copyright MBE, Stenberg et al. 2003).

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In Dahlica triquetrella diploid sexual females have a very low capacity for tychoparthenogenesis (occasional parthenogenesis). All females lay unfertilized eggs when they fail to mate, but very few eggs develop further this way (Seiler and Puchta 1956); ∼15 out of 4000 eggs studied from different populations (Seiler 1959). The asexual embryos are formed through automictic mechanism called centric fusion (Seiler and Schäffer 1960; Seiler 1963). Since the oogenesis of lepidopterans is achiasmate, there is no crossing over and no concomitant erosion of heterozygosity (Suomalainen et al. 1987). Accordingly, the mechanism transfers the entire genotype as a whole from one generation to the next one. The clonal forms are either diploid or tetraploid. Diploid parthenogenetic females have either XY or X0 sex chromosomes (Seiler 1959) and in many populations parthenogenesis seems to be unstable (Seiler and Schäffer 1960). In fact, in unstable populations the oogenesis of a diploid parthenogen is subject to a competitive inhibition: in an unfertilized egg the process of central fusion produces offspring and the egg nucleus is discarded. If the egg is fertilized, the egg nucleus takes over. In the stable diploid parthenogenetic lineages, however, fertilization does not take place and egg development is always asexual (Seiler 1963). Tetraploids are always stable and have lost the Y chromosome (Seiler 1963), they are produced through nuclear fusions before the blastoderm stage during embryogenesis in stable diploid parthenogenetic lineages (Seiler 1964). Seiler showed that triploid hybrids between tetraploid parthenogens and diploid males are intersex and sterile (Seiler et al. 1958). Seiler and his colleagues have, in our opinion, convincingly shown that D. triquetrella has the ability to spontaneously produce automictic diploids that may give rise to tetraploid parthenogenetic females through autopolyploidization and that these most likely are polyphyletic (Seiler 1965; Lokki et al. 1975).

The geographical distribution of different forms of D. triquetrella conforms to geographical polyploidy. Diploid sexual populations may be found in the foothills of the Alps, diploid parthenogens have spread over a rather limited territory to surrounding lower mountain areas, while the tetraploids have reached the high Alps and spread all the way to central Scandinavia in the north and North America in the west (Fig. 2). All three forms are sympatric at certain sites on the Alps (Seiler 1961). Different forms of females of D. triquetrella do not have equal fitness. Diploid parthenogens lay fewer eggs than diploid sexual females but always somewhat more than a half the amount that the latter produce (Seiler and Schäffer 1960), the tetraloids produce more than either diploid form. Kumpulainen et al. (2004) have shown that hymenopteran parasitoids cause a heavier mortality among asexual than sexual Dahlica. Nevertheless, the pattern of geographical distribution shows that asexual diploids do somewhat better than conspecific sexuals, and that tetraploid asexuals do far better than either diploid form.

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Figure 2. Geographical distribution of different forms of Dahlica triquetrella in Europe. The black and white dots show localities where diploid sexuals have been found. Dark grey shading covers the distribution of diploid parthenogens and the light grey shading the distribution of tetraploid parthenogens. The North American distribution of the latter is not shown. All races can coexist at a single locality. The reader is advised to consult Seiler (1961) for details.

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Is clonal reproduction the key factor explaining geographical parthenogenesis?

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

Bierzychudek (1985) drew the conclusion that there was very little evidence for asexuality by itself explaining GP in plants. She argued that polyploidy was a more parsimonious explanation for the patterns of distribution. As stated in the introduction, all asexual angiosperms are polyploid but there are also sexually reproducing polyploids. Stebbins (1950) and Levin (1983) showed through a set of examples that polyploidisation may adapt plants to conditions other than their diploid progenitors are adapted to (de Bodt et al. 2005). Levin (1983) further discussed the role of hybridity drawing the conclusion that the effects of polyploidisation and hybridisation are not exclusive. Rather, the effect of polyploidy should be enhanced if based on a hybrid origin, as the level of heterozygosity is expected to be high in allopolyploids (Arnold 1997; Otto and Whitton 2000; Osborn et al. 2003).

We have surveyed all cases of GP in arthropods with obligate asexuality and known ploidy levels. There is little support for asexuality as the main explanatory factor behind the success of clones in these complexes. Of all the examined complexes almost 92% have polyploid clones, and 57% only have polyploid clones while 8% only have diploid ones. The sole case where asexuality alone can be identified as the single explanation is P. subaptera. One should not overlook the importance of heightened dispersal ability that clonal reproduction gives a colonizing animal, but in the few taxa where distributions of clones with different ploidy are known dispersal ability does not seem to be the factor limiting diploid clones (Seiler 1961; Adamowicz et al. 2002; Stenberg et al. 2003). Our survey shows that in the majority of cases the effects of polyploidy or hybrid origin may indirectly select for asexuality. Further, we observe two clear cases of geographical polyploidy (O. scaber and D. triquetrella) where asexuality clearly fails to explain the geographical distribution: diploid sexuals and diploid parthenogens have essentially similar distributions. In most cases we can not discriminate between effects of ploidy level and hybrid origin as the origins of clonal forms are unknown. Of the taxa fulfilling the criteria for our survey, only D. triquetrella has been convincingly shown to be able to spontaneously give rise to clones and polyploids, and as such is our only example illustrating that a hybrid origin is not needed for GP in arthropods.

Adaptive potential in polyploids

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

Allopolyploids have a potential to give an orchestrated response using their multiple copies of homologous loci. (Adams et al. 2003) have shown that the different genomes of both newly synthesised and old natural allopolyploids of cotton are expressed in a chimerical pattern both in time and tissue within a single plant. They conclude that epigenetic effects cause this expression pattern, and predict it to be a common consequence of genomic merger. As regulatory changes like these are more often deleterious than beneficial, they are often seen to be negative consequences of polyploidisation and hybridization (Comai 2005). In the same way, hybrid dysfunction is a more likely consequence of genome merging and polyploidisation than heterosis. To an asexual organism, such a mainly gloomy outcome is, however, totally irrelevant: all clonal lineages are reproductively isolated. Whenever lucky circumstances give rise to a fit genotype that expresses heterosis, selection will assure the success of this clonal lineage without any regard to the eventual unlucky cases.

As epigenetic influences allow heritable effects to be expressed in a single step instead of through selection over generations (Lushai et al. 2003), variation in expression patterns may suffice to compensate for the disadvantage of low ability to respond to fluctuating selection in clonal organisms. An alternating expression of different genomes may also explain the unexpectedly low incorporation of mutations in old polyploid lineages, where redundant gene copies of duplicates have been thought to be under relaxed selection (Otto 2003). Although the above findings have been made on plants, the implications are important for polyploidy in animal evolution as well, as variability is one of the keys to evolutionary persistence. It may be that variation in expression patterns explains apparent host shifts commonly observed in young clonal species as e.g. O. sulcatus, where genetic variation is sparse or nonexistent (Lundmark et al., unpubl.).

The adaptive potential of polyploid genomes may also be illustrated in Palaearctic terrestrial earthworms where as much as 40% of the examined species have been found to be polyploid (Casellato 1987). The earthworms may be asexual but are commonly amphigonic (sexual hermaphrodites) and lack sex chromosomes, the major obstacle to polyploidy in other animals. The asexuals are in general polyploid, but there are sexual polyploids as well. Geographical parthenogenesis and geographical polyploidy can then be studied within a single species that has both diploid and polyploid sexual and asexual forms. To take an example, the sexual forms of the Lumbricid Eisenia nordenskioldi, have even ploidy levels (orthoploids) ranging from diploid to octoploid (2n-8n) while the only recorded parthenogen is a septaploid (7n) (Viktorov 1997). Although the sexual forms cannot self fertilize, and need to find a mate, produce male gametes etc., the distribution of each form is wider the higher the ploidy level (Grafodatsky et al. 1982; Perel and Grafodatsky 1983; Viktorov 1997). Superior dispersal ability does not explain the success of the polyploids, since all are sexual and pay the cost of sex in a like fashion.

Conclusions

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

We have surveyed the asexual invertebrate taxa with GP and known ploidy levels. There is little evidence that asexuality in itself is the only factor underlying GP. We argue that elevated ploidy explain the apparent evolutionary success better than reproductive mode in these cases.

Different authors have singled out different factors in the life of clonal and polyploid organisms, and these factors have been proposed to explain the repeated origin, survival and success of clones that manifests itself as GP in many taxa. For example Baker (1965) and Cuellar (1977) argue for reproductive assurance and dispersal ability, i.e. asexuality for itself. Haag and Ebert (2004) highlight effects of low population size such as bottlenecks, inbreeding depression and genetic drift in subdivided and marginal populations. Kearney (2005) makes a case for heterosis effects connected with hybrid origin and Comai (2005) for the buffering against deleterious mutations, both at a diploid adult stage and haploid gamete stage that organisms achieve through polyploidisation. We wonder if epigenetic variability will turn out to be as important as any of the above factors. The pattern called geographical parthenogenesis probably depends on all these factors in combination where different phenomena contribute more or less. In the invertebrate animals studied so far, however, it seem as a polyploid genome are of substantial weight.

Our conclusions here are based on the few adequately studied cases only. We call for more studies that would help untie the problems involving reproductive mode and polyploidy in combination. The importance of understanding asexual pests in our modern society with its huge crop monocultures cannot be stressed enough. To have our daily bread or clothes, we also need to understand the ways to increase the yield of polyploid wheat, potatoes or cotton.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References

We would like to thank the reviewers for valuable comments on the manuscript. We also want to thank the Swedish Research Council for Science, Nilsson-Ehle Foundation, Philip Sorensen Foundation, and the J. C. Kempe Foundation for financial support.

References

  1. Top of page
  2. Abstract
  3. Arthropod taxa with geographical parthenogenesis
  4. Is clonal reproduction the key factor explaining geographical parthenogenesis?
  5. Adaptive potential in polyploids
  6. Conclusions
  7. Acknowledgements
  8. References
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