Evolutionary genetics and ecology of sperm-dependent parthenogenesis

Sperm-dependent (or pseudogamous) forms of parthenogenetic reproduction occur in a wide variety of animals. Inheritance is typically clonal and matroclinous (of female descent), but sperm are needed to initiate normal development. As opposed to true parthenogenesis (i.e., sperm-independent reproduction), pseudogamous parthenogenetic lineages must coexist with a ‘sperm donor’— e.g., males from a conspecific sexual lineage, conspecific hermaphrodites, or males from a closely related sexual species. Such sperm donors do not contribute genetically to the next generation. The parasitic nature of sperm-dependent parthenogenesis raises numerous ecological and evolutionary questions. How do they arise? What factors help stabilize coexistence between the pseudogamous parthenogens and their sperm donors (i.e., ‘sexual hosts’)? Why do males waste sperm on the asexual females? Why does true parthenogenesis not evolve in pseudogamous lineages and free them from their dependency on sperm donors? Does pseudogamous parthenogenesis provide compensatory benefits that outweigh the constraints of sperm-dependence? Herein, we consider some genetic, ecological, and geographical consequences of sperm-dependent parthenogenesis in animals.     

Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogenetic females

Abstract. Stimuli associated with copulatory behavior are often needed to maximize reproductive output in internally fertilized sexual taxa. Although non-pseudogamous parthenogenetic females have no need for sperm, parthenogens descended from sexual ancestors may still require copulatory stimuli to reach their full reproductive potential. Retention of physiological dependence on copulation in parthenogens could facilitate the maintenance of sexual reproduction in species where sexual and parthenogenetic individuals coexist if parthenogens do not receive enough copulatory stimuli to achieve maximal daughter production. A laboratory experiment was conducted to determine whether embryo production in parthenogenetic female snails ( Potamopyrgus antipodarum ) is dependent on male presence. Rather than male presence, this experiment showed that embryo production is affected by the number of coexisting parthenogens. Specifically, parthenogens housed with fewer other parthenogens produced significantly more embryos than parthenogens housed with a greater number of other parthenogens, regardless of male presence and total population size. This result indicates that copulatory dependence is not likely to contribute to the maintenance of sex in P. antipodarum . Instead, it demonstrates that females of P. antipodarum negatively affect each other's reproduction, and suggests that females of P. antipodarum may exert a larger competitive influence than males of P. antipodarum . Moreover, this finding raises the possibility that highly parthenogenetic and consequently female-dense populations of P. antipodarum may experience decreased reproductive output when population size is large and resources are limiting.     

Sperm length and quality in sperm-dependent parthenogens

Is the male function of parthenogenetic hermaphrodites a historic remnant or an adaptive investment? In the first case, one would expect the male function to be ‘degraded’ and, in the second case, fully functional, despite being reduced. To answer this question, we investigated sperm morphology and quality in the hermaphroditic planarian Schmidtea polychroa. Parthenogenetic forms of this species are sperm‐dependent and require allosperm to trigger embryogenesis. Although there is generally no genetic paternal contribution, occasional fertilization of parthenogenetic eggs has been reported, leading to genetic changes in an otherwise apomictic lineage (‘occasional sex’). Comparing two locations, one with pure clonality and one with occasional sexuality, revealed substantial differences in both sperm length and fertility: Occasional sex appears to be coupled with longer sperm and higher sperm quality. We discuss the implications of these results for the maintenance of the male function in sperm‐dependent parthenogens. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93 , 81–87.     

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. This revised version was published online in July 2006 with corrections to the Cover Date.     

Characterization of polymorphic microsatellite markers in the brine shrimp Artemia (Branchiopoda, Anostraca)

The brine shrimp Artemia is a complex genus containing sexual species and parthenogenetic lineages. Artemia franciscana is native to America and its cysts (diapausing eggs) are used worldwide as a food source in aquaculture. As a consequence, this anostracan has become an invasive species in many hypersaline aquatic ecosystems of other continents. Parthenogenetic Artemia lineages occur only in the Old World. Ten and five microsatellite markers were developed to characterize two populations for A. franciscana and two populations for diploid parthenogenetic Artemia, respectively. For A. franciscana the number of alleles ranged from 11 to 58 per locus, while for parthenogens the number of alleles ranged from three to 10. The levels of heterozygosity in A. franciscana and in parthenogens ranged from 0.115 to 0.976 and from 0.000 to 0.971, respectively. These microsatellite loci showed a high population assignment power, which will be useful for future studies of population genetics and invasive processes in Artemia.     

Multiple supernumerary chromosomes in the pseudogamous parthenogenetic flatworm Polycelis nigra: lineage markers or remnants of genetic leakage?

Polycelis nigra is a free-living simultaneous hermaphroditic flatworm that has amphimictic and pseudogamous parthenogenetic biotypes. Sexual individuals are always diploid (2n = 16) and pseudogamous parthenogens are polyploid (usually triploid). Two types of supernumerary chromosomes are found in parthenogens, those resembling autosomes ("A-like") and typical B chromosomes, both of which reach frequencies in populations of close to 100%. Experiments measuring the transmission rates of the B chromosomes indicated that they are potentially inherited via the male line, escaping expulsion by pseudogamous parthenogenesis. This study used the C-banding technique to demonstrate (i) that there is a single morphologically distinct B chromosome (B1) and (ii) that there are two "A-like" chromosomes that can be considered B chromosomes (B2 and B3) and which are not simple polysomics of one of the eight autosomes. As there is no genetic exchange between pseudogamous parthenogenetic lineages, two different individuals carrying a similar B morph must either have received it through common ancestry (a lineage marker) or have acquired it horizontally from another parthenogenetic lineage (leakage). C-banding further revealed intra-individual heteromorphy for band regions on chromosomes 5 and 8. This supports the karyotypic observation that oogenesis is preceded by premeiotic chromosome doubling followed by pairing of replicate homologues.     

Population structure, parasitism, and survivorship of sexual and autodiploid parthenogenetic Campeloma limum

Two theories for the maintenance of sexual reproduction, the Red Queen hypothesis and mutation accumulation, suggest that the dispersal rates of sexuals and asexuals may determine the elimination or persistence of asexuals. Under higher dispersal rates of asexuals, asexuals may temporarily escape virulent parasites and reduce the effects of deleterious mutations. In the present study, I examine the population structure, parasite loads, and juvenile survivorship of Campeloma limum sexuals and autodiploid parthenogens from the southeastern U.S. Atlantic coastal plain. Using mtDNA sequence variation, it is shown that parthenogenetic haplotypes with limited sequence divergence are geographically widespread throughout this region and there is no significant population differentiation over a broad geographical scale. Sexual C. limum populations show significant mtDNA differentiation among and within river drainages and there is significant isolation by distance. These patterns are consistent with a recent origin and range expansion of parthenogens. Prevalence of infection by digenetic trematodes is significantly higher in autodiploid parthenogens, and the variance of prevalence is also higher in autodiploid parthenogens. I argue that the latter pattern indicates that unparasitized parthenogens have temporarily escaped these virulent parasites, but recolonization of these populations by trematodes results in high infection levels (> 40%), possibly due to reduced variation in resistance genes. I also examined whether the survivorship of juvenile sexuals and parthenogens varied under different stress levels. Sexual juveniles had twofold higher survivorship in all environments. Compared to polyploid parthenogens, autodiploid parthenogens may be less buffered against the effects of deleterious recessive alleles. I propose that the combined effects of higher parasitism and reduced juvenile survivorship of these autodiploid parthenogens accounts for the spatial distribution of sexual and parthenogenetic C. limum in the Atlantic coastal plain. Parthenogens may persist by higher dispersal rates into marginal habitats where there is a temporary escape from digenetic trematodes and competition with sexuals.     

Lower fecundity in parthenogenetic geckos than sexual relatives in the Australian arid zone

Theoretical models of the advantage of sexual reproduction typically assume that reproductive output is equal in sexual and parthenogenetic females. We tested this assumption by comparing fecundity between parthenogenetic and sexual races of gekkonid lizards in the Heteronotia binoei complex, collected across a 1200 km latitudinal gradient through the Australian arid zone. Under laboratory conditions, parthenogenetic geckos had approximately 30% lower fecundity when compared with their sexual progenitors, irrespective of body size. Reflecting clutch-size constraints in gekkonids, this fecundity difference was mainly because of fewer clutches over a shorter period. When parthenogens were compared more broadly with all coexisting sexual races across the latitudinal gradient, parthenogens had lower fecundity than sexuals only when corrected for body size. Differences in fecundity between parthenogens and coexisting sexual races depended on which sexual race was considered. There was no significant relationship between fecundity and parasite (mite) load, despite significantly higher mite loads in parthenogens than in sexual races.     

Low parasitism rates in parthenogenetic bagworm moths do not support the parasitoid hypothesis for sex

The parasite hypothesis for sex is one of the many theories that have been suggested to solve the mystery of the widespread occurrence of sex despite its high short‐term costs. It suggests that sexual lineages have an evolutionary advantage over parthenogens because they can frequently generate new genotypes that are temporarily less prone to coevolving parasites. In this study, we looked for further supporting evidence for the parasite hypothesis of sex in an attempt to understand the coexistence of sexual and parthenogenetic bagworm moths (Naryciinae). The bagworm moths and their parasitoids form one of the few natural host–parasite systems where sexual and parthenogenetic hosts are apparently not separated by ecological or geographical barriers. Furthermore, in support of the parasite hypothesis for sex, parthenogenetic presence is negatively correlated with parasitism rate. We specifically tested, by identifying the reproductive mode of the parasitized individuals, whether parasitoids preferentially attack the parthenogens in sites with both sexual and parthenogenetic forms, as predicted by the parasite hypothesis. We collected hosts from sites with different frequencies of parthenogenetic and sexual moths. A DNA barcoding approach was used to determine the reproductive mode of the parasitized hosts. Furthermore, we investigated whether differences in host and parasitoid phenology could provide an alternative explanation for the variation in parasitism rates between parthenogens and sexuals. Our results contradict the prediction of the parasite hypothesis because parthenogenetic bagworm moths were less parasitized than sexuals in sympatric sites. Our findings can be explained by differences in phenology between the parthenogenetic and sexual moths rather than genetic incompatibility between parthenogenetic hosts and parasitoids. The stable coexistence of sexual and parthenogenetic Naryciinae despite the many apparent costs of sex in this system remains a mystery. Our work adds to the list of studies were the assumptions of the parasite hypothesis for sex are not all met.     

Main role of self-pollination rate on reproductive allocations in pseudogamous apomicts

 Most apomicts are hermaphroditic and pseudogamous (pollination is necessary to trigger parthenogenesis). In these plants, fitness depends on the number of progeny obtained by maternal reproduction. We determined the evolutionary stable strategy for male and female sex allocation. We show that the efficiency of pollination determines male and female resource allocations. Predictions are made of these allocations, of pollen/ovule ratio and of seed-set. We show that self-compatibility in apomicts is necessary for the maintenance of an apomictic population, and thus can account for the association between the loss of self-incompatibility and pseudogamous apomixis. In contrast to sexuals, male investment in pseudogamous apomicts increases with the rate of self-pollination. Received: 15 June 1996 / Accepted: 20 September 1996     

Comparing fecundity in parthenogenetic versus sexual populations of the freshwater snail Campeloma limum: is there a two‐fold cost of sex?

Abstract. The predominance of sexuality in eukaryotes remains an evolutionary paradox, given the "two-fold cost of sex" also known as the "cost of males." [Correction added after online publication 29 January 2009: in the preceding sentence, extraneous words were deleted.] As it requires two sexual parents to reproduce and only one parthenogenetic parent, parthenogens should have twice the reproductive rate compared with their sexual counterparts and their genes should spread twice as fast, if all else is equal. Yet, parthenogenesis is relatively rare and considered an evolutionary dead-end, while sexuality is the dominant form of reproduction in multicellular eukaryotes. Many studies have explored short-term benefits of sex that could outweigh its two-fold cost, but few have compared fecundity between closely related sexuals and parthenogens to first verify that "all else is equal" reproductively. We compared six fecundity measures between sexual and parthenogenetic populations of the freshwater snail, Campeloma limum , during a brooding cycle (1 year) across two drainages. Drainages were analyzed separately because of a significant drainage effect. In the Savannah drainage, fecundity was not significantly different between sexuals and parthenogens, even though parthenogens had significantly more empty egg capsules per brood. In the Ogeechee drainage, parthenogens had significantly more egg capsules with multiple embryos and more hatched embryos than sexuals. Taken over 1 year, embryo size was not significantly different between parthenogens and sexuals in either drainage. Given these results and the close proximity of sexual and parthenogenetic populations, it is perplexing why parthenogenetic populations have not completely replaced sexual populations in C. limum.     

Increased capacity for sustained locomotion at low temperature in parthenogenetic geckos of hybrid origin

The evolution of parthenogenesis is typically associated with hybridization and polyploidy. These correlates of parthenogenesis may have important physiological consequences that need be taken into account in understanding the relative merits of sexual and parthenogenetic reproduction. We compared the thermal sensitivity of aerobically sustained locomotion in hybrid/triploid parthenogenetic races of the gecko Heteronotia binoei and their diploid sexual progenitors. Endurance times at low temperature (10 degrees , 12.5 degrees , and 15 degrees C, 0.05 km h(-1)) were significantly greater in parthenogenetic females than in sexual females. Comparison of oxygen consumption rates during sustained locomotion at increasing speeds (0.05, 0.10, 0.15, 0.20, 0.25, and 0.30 km h(-1), 25 degrees C) indicated that parthenogenetic lizards have higher maximum oxygen consumption rates and maximum aerobic speeds than do female sexual geckos. In addition, parthenogenetic geckos showed greater levels of voluntary activity at 15 degrees C than did sexual geckos, although this pattern appears strongest in comparison to male sexual forms. Parthenogenetic lineages of Heteronotia thus have an advantage over sexual lineages in being capable of greater aerobic activity. This result is opposite of that found in prior studies of parthenogenetic teiid lizards (genus Cnemidophorus) and highlights the idiosyncratic nature of phenotypic evolution in parthenogens of hybrid origin.     

Obligate asex in a rotifer and the role of sexual signals

Transitions to asexuality have occurred in many animals and plants, yet the biological mechanisms causing such transitions have often remained unclear. Cyclical parthenogens, such as cladocerans, rotifers or aphids often give rise to obligate asexual lineages. In many rotifers, chemical signals that accumulate during population crowding trigger the induction of sexual stages. In this study, I tested two hypotheses on the origin of obligate parthenogenesis in the rotifer Brachionus calyciflorus: (i) that obligate parthenogens have lost the responsiveness to the sexual signal; and (ii) that obligate parthenogens have lost the ability to produce the sexual signal. Pairwise cross-induction assays among three obligate parthenogenetic strains and two cyclically parthenogenetic (sexual) strains were used to test these hypotheses. I found that obligate parthenogens can induce sexual reproduction in sexual strains, but not vice versa. This demonstrates that obligate parthenogens do still produce the sexual signal, but have lost responsiveness to that signal.     

Paternal sex in parthenogenetic planarians: a tool to investigate the accumulation of deleterious mutations

Clonally reproducing organisms are expected to accumulate slightly deleterious mutations, and this has been demonstrated in RNA viruses, bacteria and unicellular algae. In this paper we present evidence for increased embryo mortality in obligate parthenogenetic strains of the freshwater flatworm Schmidtea polychroa, possibly indicating the action of deleterious mutations. The inheritance of this fitness defect was tested by crossing parthenogens with sexuals. This is possible because both forms are simultaneous hermaphrodites that produce fertile sperm. The resulting sexual offspring showed significantly increased embryo mortality in comparison to offspring of a sexual × sexual cross. Alternatives to a mutation explanation of these results, like the degeneration of male traits in parthenogens, are being discussed. In conclusion, these results lend support to the hypothesis that sex is advantageous to a multicellular organism because it prevents the accumulation of deleterious mutations.     

The cost of sex and competition between cyclical and obligate parthenogenetic rotifers

The ubiquity of sexual reproduction is an evolutionary puzzle because asexuality should have major reproductive advantages. Theoretically, transitions to asexuality should confer substantial benefits in population growth and lead to rapid displacement of all sexual ancestors. So far, there have been few rigorous tests of one of the most basic assumptions of the paradox of sex: that asexuals are competitively superior to sexuals immediately after their origin. Here I examine the fitness consequences of very recent transitions to obligate parthenogenesis in the cyclical parthenogenetic rotifer Brachionus calyciflorus. This experimental system differs from previous animal models, since obligate parthenogens were derived from the same maternal genotype as cyclical parthenogens. Obligate parthenogens had similar fitness compared with cyclical parthenogens in terms of the intrinsic rate of increase (calculated from life tables). However, population growth of cyclical parthenogens was predicted to be much lower: sexual female offspring do not contribute to immediate population growth in Brachionus, since they produce either males or diapausing eggs. Hence, if cyclical parthenogens constantly produce a high proportion of sexual offspring, there is a cost of sex, and obligate parthenogens can invade. This prediction was confirmed in laboratory competition experiments.     

Parthenogenetic flatworms have more symbionts than their coexisting,sexual conspecifics,but does this support the Red Queen?

The Red Queen hypothesis predicts that sexuality is favoured when virulent parasites adapt quickly to host genotypes. We studied a population of the flatworm Schmidtea polychroa in which obligate sexual and parthenogenetic individuals coexist. Infection rates by an amoeboid protozoan were consistently higher in parthenogens than in sexuals. Allozyme analysis showed that infection was genotype specific, with the second most common clone most infected. A laboratory measurement of fitness components failed to reveal high infection costs as required for the Red Queen. Although fertility was lower in more infected parthenogens, this effect can also be explained by the accumulation of mutations. We discuss these and other characteristics of our model system that may explain how a parasite with low virulence can show this pattern.     

Environmental stability and the distribution of the sexes: insights from life history experiments with the geographic parthenogen Eucypris virens (Crustacea: Ostracoda)

In many species with mixed reproduction, parthenogens cover a wider geographic range than sexuals. In freshwater ostracods this pattern referred to as geographic parthenogenesis is traditionally explained by ascribing a higher potential for dispersal to parthenogens. For example, the postglacial invasion hypothesis states that the lack of males in northern Europe is caused by the relatively slow range expansion of sexual lineages after deglaciation. An alternative explanation for the contemporary distribution of the sexes is based on spatial and temporal variations in ecological habitat stability. To test this hypothesis, we compared life history data of Eucypris virens individuals originating from bisexual and all-female populations. Populations with males are only found around the Mediterranean, whereas parthenogens cover most of Europe. The animals were hatched and grown in environments mimicking temperature and photoperiod conditions observed in Belgium and Spain. The data confirm the higher potential for population growth in parthenogens. In particular their faster hatching response, possibly higher fecundity (as derived from a difference in body height) and the absence of a cost of males should allow them to out-compete sexuals under stable conditions. However, the comparison of the hatchling accumulation curves of bisexual and all-female populations suggests that sexuals have an advantage in highly unpredictable environments. Indeed, under conditions mimicking those in southern Europe, bisexual populations exhibit a bet-hedging strategy, while parthenogenetic resting eggs hatch on average earlier and more synchronously. Overall, the life history data stress the importance of short term environmental fluctuations for the distribution of the sexes in E. virens , and probably many other inhabitants of ephemeral water bodies.     

Ant queens adjust egg fertilization to benefit from both sexual and asexual reproduction

An enduring problem in evolutionary biology is the near ubiquity of sexual reproduction despite the inherent cost of transmitting only half the parent's genes to progeny. Queens of some ant species circumvent this cost by using selectively both sexual reproduction and parthenogenesis: workers arise from fertilized eggs, while new queens are produced by parthenogenesis. We show that queens of the ant Cataglyphis cursor maximize the transmission rate of their genes by regulating the proportion of fertilized and parthenogenetic eggs laid over time. Parthenogenetic offspring are produced in early spring, when workers raise the brood into sexuals. After the mating period, queens lay mostly fertilized eggs that will be reared as the non-reproductive caste.     

Mode of origin differentially influences the fitness of parthenogenetic freshwater snails

How parthenogenetic lineages arise from sexual ancestors may strongly influence their persistence over evolutionary time. Hybrid parthenogens often have elevated heterozygosity and ploidy, thus making it difficult to disentangle the influence of reproductive mode, hybridity and ploidy on their relative fitness. By comparing the relative fitness of both hybrid and non-hybrid parthenogens to their sexual ancestors, further insight may be gained into how these three factors influence the maintenance of sexual and parthenogenetic reproduction. In the present study, hybrid and non-hybrid parthenogenetic and sexual snails (Campeloma sp.) were compared for the following characteristics: female size-fecundity curves, offspring size, survivorship, and growth. Compared to nearby sexual populations, triploid hybrid parthenogens from the Florida Gulf coast have similar fecundity and offspring size, five-times higher survivorship, and 60% higher growth. Relative to nearby sexual populations, non-hybrid parthenogenetic C. limum from the Atlantic coast have significantly higher fecundity, smaller offspring size, similar survivorship and slightly lower growth. Given the considerable fitness advantages of parthenogens, especially hybrid parthenogens, it is enigmatic as to why these parthenogens occupy marginal natural habitats.     

Physiological implications of genomic state in parthenogenetic lizards of reciprocal hybrid origin

Parthenogenesis often evolves in association with hybridization, but the associated ecological consequences are poorly understood. The Australian gecko Heteronotia binoei is unusual because triploid parthenogenesis evolved through reciprocal crosses between two sexual lineages, resulting in four possible cytonuclear genotypes. In this species complex, we compared the performance of these parthenogenetic genotypes with their sexual progenitors for a suite of physiological traits (metabolic rate, thermal tolerance, locomotor performance, and in vitro activity and gene sequence divergence of a cytonuclear metabolic pathway, cytochrome C oxidase). Mass‐specific metabolic rate scaled differently with body mass for parthenogens and sexuals, while heat tolerance provided the only evidence for cytonuclear incompatibility in hybrid parthenogens. The most prominent phenotypic effects were attributable to nuclear genome dosage. Overall, our results suggest that the hybrid/polyploidy origin of parthenogenetic H. binoei has had surprisingly few negative fitness consequences and may have produced a broader overall niche for the species.