Maternal sex effects and inbreeding depression under varied environmental conditions in gynodioecious Fragaria vesca subsp. bracteata

Background and Aims

Gynodioecy (coexistence of females and hermaphrodites) is a sexual system that occurs in numerous flowering plant lineages. Thus, understanding the features that affect its maintenance has wide importance. Models predict that females must have a seed fitness advantage over hermaphrodites, and this may be achieved via seed quality or quantity. Females in a population of Fragaria vesca subsp. bracteata, a long-lived gynodioecious perennial, do not demonstrate a seed quantity advantage, so this study explored whether females produced better quality seed via maternal sex effects or avoidance of inbreeding depression (IBD).

Methods

Families of selfed and outcrossed seed were created using hermaphrodite mothers and families of outcrossed seed were created using female mothers. The effects of these pollination treatments were assessed under benign conditions early in life and under varied conditions later in life. To test for an effect of maternal sex, fitness components and traits associated with acclimation to variable environments of progeny of outbred hermaphrodites and females were compared. To test for expression of IBD, fitness parameters between inbred and outbred progeny of hermaphrodites were compared.

Key Results

Offspring of females were more likely to germinate in benign conditions and survive in harsh resource environments than outbred progeny of hermaphrodites. IBD was low across most life stages, and both the effect of maternal sex on progeny quality and the expression of IBD depended on both maternal family and resource condition of the progeny.

Conclusions

The effect of maternal sex and IBD on progeny quality depended on resource conditions, maternal lineage and progeny life stage. In conjunction with known lack of differences in seed quantity, the quality advantages and IBD observed here are still unlikely to be sufficient for maintenance of gynodioecy under nuclear inheritance of male sterility.     

Gain-of-Function Mutations of fem-3, a Sex-Determination Gene in Caenorhabditis elegans

We have isolated nine gain-of-function (gf) alleles of the sex-determination gene fem-3 as suppressors of feminizing mutations in fem-1 and fem-2. The wild-type fem-3 gene is needed for spermatogenesis in XX self-fertilizing hermaphrodites and for male development in both soma and germ line of XO animals. Loss-of-function alleles of fem-3 transform XX and XO animals into females (spermless hermaphrodites). In contrast, fem-3(gf) alleles masculinize only one tissue, the hermaphrodite germ line. Thus, XX fem-3(gf) mutant animals have a normal hermaphrodite soma, but the germ line produces a vast excess of sperm and no oocytes. All nine fem-3(gf) alleles are temperature sensitive. The temperature-sensitive period is from late L4 to early adult, a period just preceding the first signs of oogenesis. The finding of gain-of-function alleles which confer a phenotype opposite to that of loss-of-function alleles supports the idea that fem-3 plays a critical role in germ-line sex determination. Furthermore, the germ-line specificity of the fem-3(gf) mutant phenotype and the late temperature-sensitive period suggest that, in the wild-type XX hermaphrodite, fem-3 is negatively regulated so that the hermaphrodite stops making sperm and starts making oocytes. Temperature shift experiments also show that, in the germ line, sexual commitment appears to be a continuing process. Spermatogenesis can resume even after oogenesis has begun, and oogenesis can be initiated much later than normal.     

Conservation of large foci formation in arrested oocytes of <Emphasis Type="Italic">Caenorhabditis</Emphasis> nematodes

Within the rhabditid phylogeny of nematodes, the great majority of species are gonochoristic, having evolved as obligate male/female species. In contrast, the well-studied nematode model system, Caenorhabditis elegans, is androdioecious, utilizing a hermaphroditic/male reproductive system. We have previously determined that in the arrested oocytes of old-aged C. elegans hermaphrodites with depleted sperm, large cytoplasmic ribonucleoprotein foci form. The formation of these foci is reversible, as they dissociate within 3 h after a male mates with the hermaphrodite, resupplying it with sperm. The functional significance of these oocyte foci is not known and previously has not been clear for a hermaphroditic species in which oocytes of young adults wait only approximately 23 min to be fertilized. One hypothesis is that the foci function to maintain maternal mRNAs in oocytes while fertilization is delayed. In this paper, we examine four gonochoristic rhabditid species: Caenorhabditis remanei, Caenorhabditis sp. CB5161, Caenorhabditis sp. PS1010, and Rhabditella axei DF5006. We demonstrate that in three of these four species, ovulation arrests in unmated females until mating occurs and large cytoplasmic foci develop in arrested oocytes. The oocyte foci contain nuclear pore proteins and, in C. remanei at least, the RNA-binding protein MEX-3 as well as RNA. We speculate that these foci maintain the integrity of ooctyes, possibly maintaining the stability or translational repression of maternal mRNAs in unmated females. We further speculate that their presence in oocytes of old-aged C. elegans hermaphrodites is due to conservation from an ancestral gonochoristic state.     

Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success

 In gynodioecious species, females contribute genes to future generations only through ovules, and to persist in populations they must have a compensatory advantage compared with hermaphrodites that reproduce via ovules and pollen. This compensation can result from greater fecundity and/or superior success of progeny from females. We examined differences in seed production and progeny success between females and hermaphrodites in the geophyte Wurmbea biglandulosa to explain the maintenance of females. Females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites but this did not necessarily result in greater fecundity, in part because seed production of females was pollen-limited. Over four years in one population, open-pollinated females produced 1.32 more seeds than open-pollinated hermaphrodites (range 1.09–1.63). In two other populations examined for one year only females produced 1.07 and 0.79 as many seeds as hermaphrodites. Seed production of open-pollinated females and hermaphrodites was only 55% and 73% that of cross-pollinated plants, respectively, indicating that both genders were pollen-limited but females more so than hermaphrodites. Open-pollinated seeds from females were 1.18–1.27 times more likely to germinate than seeds from hermaphrodites. No gender differences existed in seedling growth or survival. Hermaphrodites were self-compatible, but selfed seed set was only 80% that of crossed seed set. Crossed seed set of females and hermaphrodites did not differ. Assuming nuclear control of male sterility, relative female fitness is insufficient to maintain females at their current frequencies of 17%, and substantial female fitness advantages at later life-cycle stages are required. Received May 4, 2001 Accepted February 25, 2002     

EVOLUTION OF UNISEXUALITY IN THE HAWAIIAN FLORA: A TEST OF MICROEVOLUTIONARY THEORY

The evolution of separate sexes as a means of avoiding self-fertilization requires the controversial coexistence of large inbreeding depression and high selfing rate in the ancestral hermaphrodite population. Fitness components of adult females and hermaphrodites in nature, of their open-pollinated progeny, and of experimental selfs and outcrosses onto hermaphrodites were compared in endemic Hawaiian Bidens sandvicensis, all of whose known populations are gynodioecious, consisting of a mixture of females and hermaphrodites. Multilocus selfing rates of hermaphrodites were also estimated, and sex morph ratio monitored over four seasons in three populations of B. sandvicensis and one population of gynodioecious B. cervicata. Total mean inbreeding depression in seed set (in the glasshouse), germination rate (in an open-air nursery on Kauai), and first year survivorship and fecundity in the field were estimated as 0.94 (SE 0.04), and occurred primarily in drought months. Lower survivorship and fecundity of selfs were partially explained by their consistently smaller size. Open-pollinated seed of females had significantly lower germination rate, proportion flowering, and fecundity than outcrossed progeny of hermaphrodites, suggesting moderate biparental inbreeding in females and a lack of any non-outcrossing advantage to progeny of females. In all fitness components, open-pollinated progeny of hermaphrodites were inferior to those of females and to outcrosses, and in most components were superior to selfs. Total performance of open-pollinated progeny of females relative to those of hermaphrodites was calculated as 2.3 (SE = 0.4), but since inflorescences of females also set 20% to 50% more seed than those of hermaphrodites, their total relative ovule success was estimated as 3.2 (SE = 0.5). If inheritance of male sterility is nuclear, this superiority is sufficient to maintain females in frequencies over 20% in populations, whose actual frequencies ranged from 14% to 33%. In four populations, selfing rates of hermaphrodites, assayed in seedlings, were 0.50, 0.45, 0.25, and 0.30, but since substantial inbreeding depression occurred prior to germination, the mean selfing rate of hermaphrodite ovules exceeded 0.57. Female frequencies were significantly higher in the two populations with higher hermaphrodite selfing rate. These results suggest that inbreeding depression can exert a profound influence on the mating system of self-compatible plants on Hawaii and perhaps other oceanic islands, and can be sufficiently strong to electively favor the elimination of the male function.     

Protogynous hermaphroditism in the slinger, Chrysoblephus puniceus (Gilchrist & Thompson, 1908) (Teleosteir:Sparidae)

Hermaphroditism in the marine fishes is well documented, especially in the family Sparidae in which at least 35 species have been reported. Within this family sexuality ranges from gonochorism, through rudimentary, protogynous and protandrous hermaphroditism, to what is thought to be a single functional hermaphrodite.
A biological study of the economically valued Chrysoblephus puniceus revealed marked differences in the size of male and female fish, suggesting that this sparid undergoes sex reversal. Histology of gonads macroscopically classified as 'female', 'male' and 'hermaphrodite' were analysed. Degenerating pre-vitellogenic oocytes in the ovarian sections of hermaphroditic gonads confirm that C puniceus is a protogynous hermaphrodite.     

Functional characterization of gynodioecy in Fragaria vesca ssp. bracteata (Rosaceae)

Background and Aims

Gynodioecy is a phylogenetically widespread and important sexual system where females coexist with hermaphrodites. Because dioecy can arise from gynodioecy, characterization of gynodioecy in close relatives of dioecious and sub-dioecious species can provide insight into this transition. Thus, we sought to determine whether Fragaria vesca ssp. bracteata, a close relative to F. chiloensis and F. virginiana, exhibits the functional and population genetic hallmarks of a gynodioecious species.

Methods

We compared reproductive allocation of females and hermaphrodites grown in the greenhouse and estimated genetic diversity (allelic diversity, heterozygosity) and inbreeding coefficients for field-collected adults of both sexes using simple sequence repeat (SSR) markers. We estimated mating system and early seed fitness from open-pollinated families of both sex morphs.

Key Results

Under greenhouse conditions, females and hermaphrodites allocated similarly to all reproductive traits except flower number, and, as a consequence, females produced 30 % fewer seeds per plant than hermaphrodites. Under natural conditions, hermaphrodites produce seeds by self-fertilization approx. 75 % of the time, and females produced outcrossed seeds with very little biparental inbreeding. Consistent with inbreeding depression, seeds from open-pollinated hermaphrodites were less likely to germinate than those from females, and family-level estimates of hermaphrodite selfing rates were negatively correlated with germination success and speed. Furthermore, estimates of inbreeding depression based on genetic markers and population genetic theory indicate that inbreeding depression in the field could be high.

Conclusions

The joint consideration of allocation and mating system suggests that compensation may be sufficient to maintain females given the current understanding of sex determination. Fragaria vesca ssp. bracteata exhibited similar sex morph-dependent patterns of mating system and genetic diversity, but less reproductive trait dimorphism, than its sub-dioecious and dioecious congeners.     

FEMALE FREQUENCIES IN GYNODIOECIOUS POPULATIONS CORRELATED WITH SELFING RATES IN HERMAPHRODITES

Gynodioecious populations consist of separate hermaphroditic and female individuals. Females are at a selective disadvantage because they contribute genes to the next generation only through ovules, while hermaphrodites contribute genes through ovules and pollen. For females to be maintained in populations they must have some compensating selective advantage. The outcrossing hypothesis postulates that females are maintained because their progeny result from obligate outcrossing, whereas some of the progeny of hermaphrodites result from self-fertilization and are less fit because of inbreeding depression. If correct, the frequency of females should be positively correlated with selfing rates of hermaphrodites in populations. We found a strong positive correlation between female frequency and selfing rates of hermaphrodites (r = 0.91, P < 0.01) in eight gynodioecious populations of Hawaiian species of Bidens. Our results confirm that the obligate outcrossing of females is a major factor maintaining females in gynodioecious populations. However, the observed selfing rates are insufficient by themselves to account for the frequency of females in these populations.     

Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum

BACKGROUND AND AIMS: For the maintenance of gynodioecy (i.e. the coexistence of female and hermaphroditic plants), females need to compensate for the lack of pollen production through higher seed production or better progeny quality compared to hermaphrodites. In Geranium sylvaticum, females produce more seeds per flower than hermaphrodites. This difference in seed production might be modified by biological interactions with pollinators and herbivores that may favour one sex and thus affect the maintenance of gynodioecy. METHODS: Sexual dimorphism in flower size and flowering phenology, and in attractiveness to pollinators, pre-dispersal seed predators and floral herbivores were examined in natural populations of G. sylvaticum. KEY RESULTS: Pollinators preferred hermaphrodites 25 % more often than females in two of the three study populations, and floral herbivores attacked hermaphrodites 15 % more often than females in two of the six study populations. These preferences might be explained by the larger flower size of hermaphrodites. In contrast, seed predators did not prefer either sex. CONCLUSIONS: The data suggest that pollinator preference does not benefit females, whereas the higher floral herbivory of hermaphrodites might enhance the maintenance of females in G. sylvaticum. Thus, although the data support the view that ecological factors may contribute to the maintenance of gynodioecy, they also suggest that these contributions may vary across populations and that they may function in opposite directions.     

Hermaphroditism: What's not to like?

Hermaphroditism is rare and phylogenically in decline among animal species. The evolutionary basis for this development is not well understood. This paper focusses on self-incompatible simultaneous hermaphroditism in animals. It proposes that such hermaphroditism is not stable in sufficiently heterogeneous populations, suggesting a possible reason for why hermaphroditism is rare among evolved animal species. The argument turns on the Bateman principle, namely that male reproductive success (RS) is limited by partner availability, while female RS is not. We show that: low-quality individuals do better if female; secondary sexual differentiation may be important for understanding the existence of males; and that hermaphroditic mating is reciprocal. Reciprocity may be key to understanding promiscuity and attendant phenomena such as cryptic female choice, sperm competition and love darts-common features of hermaphroditic mating. We also argue that hermaphrodites are especially vulnerable to male violence, suggesting a reason for the rarity of trioecy. Finally, we propose that external fertilization, and the scope for streaking, may be one reason fish are the only simultaneously hermaphroditic vertebrates.     

Sex determination in the androdioecious plant Datisca glomerata and its dioecious sister species D. cannabina.

Datisca glomerata is an androdioecious plant species containing male and hermaphroditic individuals. Molecular markers and crossing data suggest that, in both D. glomerata and its dioecious sister species D. cannabina, sex is determined by a single nuclear locus, at which maleness is dominant. Supporting this conclusion, an amplified fragment length polymorphism (AFLP) is heterozygous in males and homozygous recessive in hermaphrodites in three populations of the androdioecious species. Additionally, hermaphrodite x male crosses produced 1:1 sex ratios, while hermaphrodite x hermaphrodite crosses produced almost entirely hermaphroditic offspring. No perfectly sex-linked marker was found in the dioecious species, but all markers associated with sex mapped to a single linkage group and were heterozygous in the male parent. There was no sex-ratio heterogeneity among crosses within D. cannabina collections, but males from one collection produced highly biased sex ratios (94% females), suggesting that there may be sex-linked meiotic drive or a cytoplasmic sex-ratio factor. Interspecific crosses produced only male and female offspring, but no hermaphrodites, suggesting that hermaphroditism is recessive to femaleness. This comparative approach suggests that the hermaphrodite form arose in a dioecious population from a recessive mutation that allowed females to produce pollen.     

日本血吸虫的雌雄同体两性畸形

本文报告了22条我国大陆品系日本血吸虫的雌雄同体两性畸形虫体,其中雌虫两性畸形15条,雄虫两性畸形7条,并对每条两性畸形的标本作了描述。作者对两性畸形发生的原因进行了讨论,认为哺乳类血吸虫两性畸形的发生可能是遗传的返祖现象。     

Consequences of inbreeding for offspring fitness and gender in Silene vulgaris,a gynodioecious plant

Abstract In gynodioecious plants, hermaphrodite and female plants co‐occur in the same population. In these systems gender typically depends on whether a maternally inherited cytoplasmic male sterility factor (CMS) is counteracted by nuclear restorer alleles. These restorer alleles are often genetically dominant. Although plants of the female morph are obligatorily outcrossing, hermaphrodites may self. This selfing increases homozygosity and may thus have two effects: (1) it may decrease fitness (i.e. result in inbreeding depression) and (ii) it may increase homozygosity of the nuclear restorer alleles and therefore increase the production of females. This, in turn, enhances outcrossing in the following generation. In order to test the latter hypothesis, experimental crosses were conducted using individuals derived from four natural populations of Silene vulgaris, a gynodioecious plant. Treatments included self‐fertilization of hermaphrodites, outcrossing of hermaphrodites and females using pollen derived from the same source population as the pollen recipients, and outcrossing hermaphrodites and females using pollen derived from different source populations. Offspring were scored for seed germination, survivorship to flowering and gender. The products of self‐fertilization had reduced survivorship at both life stages when compared with the offspring of outcrossed hermaphrodites or females. In one population the fitness of offspring produced by within‐population outcrossing of females was significantly less than the fitness of offspring produced by crossing females with hermaphrodites from other populations. Self‐fertilization of hermaphrodites produced a smaller proportion of hermaphroditic offspring than did outcrossing hermaphrodites. Outcrossing females within populations produced a smaller proportion of hermaphrodite offspring than did crossing females with hermaphrodites from other populations. These results are consistent with a cytonuclear system of sex determination with dominant nuclear restorers, and are discussed with regard to how the mating system and the genetics of sex determination interact to influence the evolution of inbreeding depression.     

Sexuality and hermaphroditism in fishes. I. Synchronous functional hermaphroditism in the serranid fish Serranus scriba L

Anatomical and histological examination of Serranus scriba L. showed the existence of primary females (67%), hermaphrodites (31%) and primary males (2%). Synchronous functional hermaphroditism is described on the basis of an anatomical and histological study of the gonads. Although they function simultaneously, the testicular and ovarian parts of hermaphrodite gonads have completely separate ducts. Females and hermaphrodites have the same annual reproduction cycle. In hermaphrodites, the testicular part matures one month sooner than the ovarian part. Cross fertilization between primary females and hermaphrodite individuals and between two different hermaphrodites probably occurs, while self-fertilization is less likely. The testicular tissues of primary males are of the acinar type and those of hermaphrodites are of the radial type. It is possible that primary males do not take part in reproduction. Serranus scriba in Egyptian Mediterranean waters is a longperiod spawner, which spawns from June to the end of October, i.e. it is a summer-autumn spawner.     

Simultaneous hermaphroditism; cost and benefit

Current theories explain simultaneous hermaphroditism by the advantage it gives to organisms which are widely dispersed or sluggish, resulting in a low frequency of reproductive contacts. It is difficult to see why hermaphroditism is not more widespread unless there is some counterbalancing disadvantage.It is suggested that hermaphrodites suffer an energetic cost because they maintain two reproductive systems and a cost due to the reduced number or viability of offspring which may result from accidental self-fertilization. These costs will result in a disadvantage to hermaphroditism (compared to gonochorism) when reproductive contacts are frequent. However, even in widely dispersed or sluggish organisms behavioural mechanisms may exist which increase the frequency of reproductive contacts, favouring gonochorism instead of hermaphroditism.It is argued that externally fertilizing species should as a rule be gonochoric and that species which brood their young may often be hermaphroditic. Hermaphroditism in species which form permanent male/female pairs in the breeding season could result in more zygotes being produced. However, where parental care of the young is important, it is suggested that gonochorism and sexual dimorphism may result in more progeny being reared.     

THE RELATIVE IMPORTANCE OF INBREEDING AND MATERNAL SEX IN DETERMINING PROGENY FITNESS IN SIDALCEA OREGANA SSP. SPICATA,A GYNODIOECIOUS PLANT

Gynodioecious plant populations contain both hermaphrodite and female individuals. For females to be maintained they must compensate for their loss of reproductive fitness through pollen. Females may achieve compensation by producing more and/or higher quality seeds than hermaphrodites. In this study, I investigated the independent and interactive effects of maternal sexual identity and inbreeding level on fitness of the progeny of hermaphrodites and females of Sidalcea oregana ssp.spicata. Seeds produced by selling hermaphrodites and by outcrossing or sib-crossing hermaphrodites and females, were planted in the field and greenhouse. Maternal-sex effects were substantial at the juvenile stages of the life cycle; seeds of females germinated in higher proportions and produced seedlings that grew significantly faster. Inbreeding effects were manifested primarily at the adult stage of the life cycle. Outcrossed plants were significantly larger and produced more flowers per plant than sib-crossed and selfed plants growing in the greenhouse. Progeny of hermaphrodites and females appeared to respond similarly to sib-matings. The maternal-sex effects observed in Sidalcea may have been related to cytoplasmically inherited factors and could be a driving force in the maintenance of females. Inbreeding depression could play a role in determining the fitness of both sex morphs, if females experience biparental inbreeding in the field. Frequent inbreeding of hermaphrodites may not be necessary to explain the maintenance of gynodioecy in this species.     

Life Cycle and Reproductive Potential of the Nematode Heterorhabditis bacteriophora Strain HP88

Development of the entomopathogenic nematode Heterorhabditis bacteriophora strain HP88 was studied in vivo with larvae of the greater wax moth, Galleria mellonella, as host and in vitro. At 25 C in vivo, the duration of the life cycle from egg hatch to egg hatch was 96 hours. Juvenile development took 48 hours, with the duration of each juvenile stage ranging from 8 to 12 hours. Under crowded conditions, development proceeded to the infective juvenile (IJ) stage instead of the third juvenile stage (J3). Life-cycle duration and proportion of the various developmental stages in the population were similar in in vitro and in vivo cultures. When in vivo or in vitro development was initiated from the IJ stage, only hermaphrodites developed in the first generation and males appeared only in the second generation. The average (±SD) number of progeny per hermaphrodite was 243 ± 98. The ratio of males to hermaphrodites in the second generation was 1:9.4 ± 6.8.     

An alpha-tubulin mutant demonstrates distinguishable functions among the spindle assembly checkpoint genes in Saccharomyces cerevisiae

The free-living nematode worm Caenorhabditis elegans reproduces primarily as a self-fertilizing hermaphrodite, yet males are maintained in wild-type populations at low frequency. To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. We show that the mating efficiency of C. elegans is poor compared to a dioecious species and that C. elegans males are more attracted to C. remanei females than they are to their conspecific hermaphrodites. We postulate that a genetic mutation occurred during the evolution of C. elegans hermaphrodites, resulting in the loss of an attracting sex pheromone present in the ancestor of both C. elegans and C. remanei. Our findings suggest that males are maintained in C. elegans because of the particular genetic system inherited from its dioecious ancestor and because of nonadaptive spontaneous nondisjunction of sex chromosomes, which occurs during meiosis in the hermaphrodite. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites.     

Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)

Background and Aims The coexistence of hermaphrodites and female-sterile individuals, or androdioecy, has been documented in only a handful of plants and animals. This study reports its existence in the plant species Cardamine amara (Brassicaceae), in which female-sterile individuals have shorter pistils than seed-producing hermaphrodites.Methods Morphological analysis, in situ manual pollination, microsatellite genotyping and differential gene expression analysis using Arabidopsis microarrays were used to delimit variation between female-sterile individuals and hermaphrodites.Key Results Female sterility in C. amara appears to be caused by disrupted ovule development. It was associated with a 2.4- to 2.9-fold increase in clonal propagation. This made the pollen number of female-sterile genets more than double that of hermaphrodite genets, which fulfils a condition of co-existence predicted by simple androdioecy theories. When female-sterile individuals were observed in wild androdioecious populations, their ramet frequencies ranged from 5 to 54 %; however, their genet frequencies ranged from 11 to 29 %, which is consistent with the theoretically predicted upper limit of 50 %.Conclusions The results suggest that a combination of sexual reproduction and increased asexual proliferation by female-sterile individuals probably explains the invasion and maintenance of female sterility in otherwise hermaphroditic populations. To our knowledge, this is the first report of the coexistence of female sterility and hermaphrodites in the Brassicaceae.     

Activity of the Sex-Determining Gene tra-2 Is Modulated to Allow Spermatogenesis in the C. ELEGANS Hermaphrodite

In the nematode C. elegans, there are two sexes, the self-fertilizing hermaphrodite (XX) and the male (XO). The hermaphrodite is essentially a female that makes sperm for a brief period before oogenesis. Sex determination in C. elegans is controlled by a pathway of autosomal regulatory genes, the state of which is determined by the X:A ratio. One of these genes, tra-2, is required for hermaphrodite development, but not for male development, because null mutations in tra-2 masculinize XX animals but have no effect on XO males. Dominant, gain-of-function tra-2 mutations have now been isolated that completely feminize the germline of XX animals so that they make only oocytes and no sperm and, thus, are female. Most of the tra-2(dom) mutations do not correspondingly feminize XO animals, so they do not appear to interfere with control by her-1, a gene thought to negatively regulate tra-2 in XO animals. Thus, these mutations appear to cause gain of tra-2 function in the XX animal only. Dosage studies indicate that 5 of 7 tra-2(dom) alleles are hypomorphic, so they do not simply elevate XX tra-2 activity overall. These properties suggest that in the wild type, tra-2 activity is under two types of control: (1) in males, it is inactivated by her-1 to allow male development to occur, and (2) in hermaphrodites, tra-2 is active but transiently inactivated by another, unknown, regulator to allow hermaphrodite spermatogenesis; this mode of regulation is hindered by the tra-2(dom) mutations, thereby resulting in XX females.