The relationship between genotype and phenotype is not a one-to-one mapping. Several genotypes can give rise to the same phenotype (as in developmental canalization in spite of genetic variations). Conversely, several phenotypes can correspond to the same genotype. Such phenotypic plasticity may occur in response to different environments and/or in complex life-cycles that include distinct morphs (Schlichting and Pigliucci 1998). Examples of developmental divergence between morphs of the same species include wing polyphenism in ants (Abouheif and Wray 2002) and pea aphid embryogenesis (Miura et al. 2003).
Many terrestrial nematodes such as Caenorhabditis elegans undergo one of two alternative postembryonic developmental modes, depending on environmental conditions. In unstressed conditions such as those of laboratory cultures (ample food, 20°C, uncrowded culture), C. elegans passes through four juvenile (larval) stages, called L1 to L4, that are separated by molts and lead to the reproductively active adult. In stressful conditions (starvation, high temperature and/or crowded culture), C. elegans passes through a “dauer” stage that corresponds to the third juvenile stage (Riddle et al. 1997; Fig. 1A). The decision is first made in the L1 stage to enter a pre-dauer L2d stage that then molts into a dauer larva (unless conditions “improve”). This dauer larva does not feed and displays specific metabolic activity, stress resistance and behaviour. The dauer corresponds to the infectious stage of animal parasites (Viney 1996; Riddle et al. 1997). In several Caenorhabditis species, the dauer stage is clearly associated with a phoretic behaviour towards an invertebrate host (Kiontke 1997; Baird 1999; Kiontke et al. 2002). In C. elegans, if good conditions return, the dauer will resume development to a L4d stage and the adult. Whether it has gone through dauer or not, the animals reproduce as self-fertilizing protandrous XX hermaphrodites and facultative XO males.
Some parasitic nematodes present a complex life-cycle with alternating parasitic and free-living generations, which in addition may adopt distinct modes of reproduction. These complex life-cycles have appeared convergently in several groups. For example, the mammalian parasite Strongyloides ratti (in clade IV of the nematode phylogeny in Blaxter et al. 1998) reproduces via parthenogenetic infectious females and a male/female free-living generation; the ratio of infectious versus free-living forms is controlled by environmental conditions (Viney 1996). In the insect parasite Heterorhabditis bacteriophora (in clade V in Blaxter et al. 1998, like C. elegans and Rhabditis sp. SB347), the infectious non-feeding juvenile develops in the host as a protandrous hermaphrodite and gives rise to non-infectious males and females (Dix et al. 1992; Zioni et al. 1992; Strauch et al. 1994; Burnell and Stock 2000). In such species, the parasitic generation is not easily accessible to detailed developmental analysis. For example, vulva development of the free-living generation of S. ratti has been described (Félix et al. 2000), but access to the parasitic generation has proven difficult (R. Sommer, personal communication).
I observed that in standard C. elegans culture conditions, Rhabditis sp. SB347 (Family Rhabditidae) presents two morphs with different modes of reproduction, namely a hermaphroditic generation that goes through an obligatory dauer stage, and a male/female generation with a direct development through the L3 stage (Fig. 1B). This prompted me to analyze developmental differences between the two morphs. Of particular interest was vulva development, because vulva precursor cell specification takes place during the L3 stage.
Nematodes of the family Rhabditidae, like C. elegans (Sulston and Horvitz 1977), display a quasi-invariant postembryonic cell lineage from a set of larval blast cells. The vulva is formed from Pn.p precursor cells that are born in the L1 stage. Twelve Pn.p cells are aligned along the ventral epidermis, and numbered 1 to 12 from anterior to posterior. In C. elegans, P3.p to P8.p are competent to adopt a vulval fate and therefore form the vulva competence (equivalence) group; more anterior and posterior Pn.p cells fuse in the L1 stage with the large syncytial epidermis hyp7 that surrounds the animal. A spatial pattern of vulval fates is then established among P(3–8).p during the L3 stage. P6.p adopts a central vulval fate or 1° (primary) fate, and P5.p and P7.p adopt a lateral vulval or 2° (secondary) fate. Finally, P3.p, P4.p and P8.p adopt a non-vulval or 3° (tertiary) fate: they divide once and fuse with the hyp7 syncytium (Fig. 2A). This pattern is primarily induced by signaling from a specialized cell of the ventral uterus called the anchor cell (AC). Laser ablation of this cell in the early L3 stage results in all P(3–8).p adopting a 3° non-vulval fate (Kimble 1981). The anchor cell signal may act as a morphogen (Katz et al. 1995) and lateral signaling from P6.p to its neighbours inhibits the 1° fate and activates their 2° fate (Sternberg 1988; Koga and Ohshima 1995; Simske and Kim 1995; Fig. 3A). At the time of Pn.p division, laser ablation of the AC has no further effect on 1°/2°/3° specification.
Other species of the family Rhabditidae present differences in the size of the vulval competence group, in patterning mechanisms and in vulval lineage (for reviews see Sommer 1996, 2000; Félix 1999). For example, several species use a nested two-step induction mechanism that results in the same final pattern of vulval fates as in C. elegans: the anchor cell first induces P(5–7).p in the early L3 stage to adopt a vulval versus non-vulval fate and then induces P6.p daughters at the end of the L3 stage to a central vulval fate (Félix and Sternberg 1997).
Here I describe the occurrence of two morphs in Rhabditis sp. SB347, and show that they display heterochrony in gonadal development and differences in vulval cell lineage and patterning mechanisms.
Materials and methods Strain and cultureThe strain Rhabditis sp. SB347 (Nematoda: Rhabditidae) was a kind gift of Drs. W. Sudhaus and K. Kiontke. The nematode was found on ticks (Ixodes scapularis) dropped to the soil (as nematode traps) in Kingston, R.I., United States by Dr. Elyes Zhioua (W. Sudhaus, personal communication).
The strain was cultured at 20°C on standard NGM plates seeded with the Escherichia coli OP50 strain, as for C. elegans (Wood 1988).
Lineage analysis and cell ablationFor cell lineage and laser ablation, worms were mounted on agar pads as described in Wood (1988) and observed by Nomarski optics with a 100× objective on a Zeiss Axioskop. Cells were ablated as described in Epstein and Shakes (1995), using a Photonic Instruments laser system.
After each cell division, the anterior daughter is designated by “a”, the posterior daughter by “p”. For example, Z1.a is the anterior daughter of Z1 (Sulston and Horvitz 1977; Kimble and Hirsh 1979). The “x” in Z1.ppx refers to both daughters of Z1.pp. Cells are scored as adopting a vulval fate when their progeny form an invagination in the L4 stage.
Results Two alternative morphs in Rhabditis sp. SB347Rhabditis sp. SB347 displays the following two developmental morphs, which correspond to alternative modes of sexual reproduction.
Males and females develop through four feeding juvenile (larval) stages called L1 to L4 (like well-fed C. elegans; Fig. 1). The generation only takes 2.5–3 days at 20°C in our culture conditions.
Hermaphrodites develop through an obligatory non-feeding third juvenile stage, the dauer larva (Fig. 1B, bottom). Dauer larvae stand up on their tail and display a characteristic solitary tube waving behaviour that may correspond to a searching behaviour for a carrier invertebrate, as found in species of Rhabditella and Cephaloboides (Sudhaus 1976; Kiontke 1999). They remain within their L2 cuticle, opening a hole at the front end, and use it as a tube into which they can retract. Lateral ridges (alae) can be found on these tubes and not on L2d animals, suggesting that some cuticular material has been added to the L2d cuticle during the L2d to dauer molt. When dauer larvae of the same age are left on food, exit from the dauer stage generally occurs after about 24 h (although not simultaneously in all individuals), in which case the generation time takes about 4 days. The dauer stage is thus only transient. The dauer larva first exits the L2d cuticle, then opens its mouth and the “L3d” program of gonadal (and later vulval) divisions resumes, starting with divisions of the ovary sheath/spermatheca lineage (which occurs either before or after mouth opening). Spermatogenesis occurs in the L4d stage, and oogenesis proceeds throughout adulthood.
Alternative developments in Caenorhabditis elegans versus Rhabditis sp. SB347. A C. elegans adopts a continuous development through the L3 stage in standard culture conditions; an alternative development through the dauer stage can be induced in the L1 stage by crowding, low food, or high temperatures. B In standard culture conditions, Rhabditis sp. SB347 can adopt two alternative developmental pathways with different modes of reproduction. These two pathways are already specified at hatching, since the gonad primordium is smaller in the young juveniles that will go through the dauer stage than in juveniles that will pass through a feeding L3 stage
In standard culture conditions (as described in Materials and methods), both morphs coexist. Because most animals are hermaphrodites, the presence of females was at first not detected in the cultures. However, three types of interindividual variations were noticed after sampling many non-male animals: size of the gonad primordium in young larvae, presence or absence of division of the P8.p cell, and presence or absence of spermatogenesis in L4 animals. These three traits are correlated in the population. For example, animals that were scored in the L4 stage for P8.p division were isolated on single plates: 12/12 animals with undivided P8.p became self-fertile hermaphrodites, whereas 7/7 animals with divided P8.p became females (they were not self-fertile and only produced progeny when a male was added to the plate). In addition, early gonadal development, P8.p division and absence of spermatogenesis correlated in all the animals that were observed during the course of ablation experiments. Male dauer larvae were never observed.
In a non-synchronized culture, 14/100 non-male animals were females (as determined by P8.p division). Single hermaphrodites give rise to hermaphrodites as well as males and females in the first generation (269 males for 2,075 animals or 13%). Single mated females also give rise to hermaphrodites as well as females and males in the first generation, but the latter in a smaller proportion (4/253 males or 1.6%). Males (and probably females) are thus more frequent in the progeny of hermaphrodites than in the progeny of a male/female pair, but generations do not strictly alternate. Because males and females do not go through the dauer stage and thus develop faster than their hermaphrodite siblings, they are greatly enriched in the F2 progeny of a hermaphrodite or a male/female pair at day 6 after their isolation of these grand-parents. For example, in the F2 progeny of mated females, 6 days after mating, 46/47 non-male L4 animals were females. Enrichment of males and females is clearly observed in these specific conditions, whereas, as mentioned above, only a few are visible in a non-synchronized culture.
Heterochrony in somatic gonad developmentIn females and males, the somatic gonadal precursors Z1 and Z4 begin their divisions in the middle of the L1 stage (Fig. 4A, B), as in C. elegans, and give rise to 12 cells (Kimble and Hirsh 1979). In females, Z1.pp and Z4.aa divide last, around the L1 to L2 molt, and give rise to four ventral uterine cells, one of which will become the anchor cell (AC) during the L2 stage. The AC can then be distinguished from the three ventral uterine precursors (VU) by morphological features such as the smaller size of its nucleus. Gonadal divisions resume in the L3 stage. So far, this timing corresponds to that described in C. elegans (Kimble and Hirsh 1979). However, the relative timing of gonadal and vulval divisions differs in the L3 stage from that of C. elegans: the VU precursors divide before the Pn.p cells in C. elegans and after the Pn.p cells in SB347 females.
In SB347 hermaphrodites, Z1 and Z4 divide in the middle of the pre-dauer L2d stage, one full larval stage later than in females (Figs. 1B, 4E), and Z1.pp and Z4.aa divide around the time of entry into dauer. The AC can be morphologically distinguished by its small size when the worms exit the dauer stage. Gonadal divisions then resume and, unlike in females but as in C. elegans, the VU precursors divide before the Pn.p cells.
Vulval precursor cell lineages in females and hermaphroditesThe vulval lineages of females and hermaphrodites of Rhabditis sp. SB347 are shown in Fig. 2B. The outer vulval precursors P5.p and P7.p divide twice (UUUU lineage). The inner precursor P6.p divides twice and its outer granddaughters divide an additional time transversally (left-right; TUUT lineage). This is an unusual lineage for P6.p in the family Rhabditidae: in all other species studied so far, the inner P6.p granddaughters divide transversally as well (Sommer and Sternberg 1995; A. Barrière and M.-A. Félix, unpublished).
Fig. 2Vulval cell lineages in C. elegans hermaphrodites (A) and Rhabditis sp. SB347 females and hermaphrodites (B). The Pn.p vulval precursor cells in the ventral epidermis divide at the end of the L3/L3d stage. S Syncytial (non-vulval) epidermal fate, T transverse division of a Pn.p granddaughter (vulval fate), L longitudinal division of a Pn.p granddaughter (vulval fate), U undivided granddaughter of a Pn.p cell (vulval fate). In Rhabditis sp. SB347 females, P8.p is the first cell of the competence group to divide; P4.p is competent (from ablation experiments; Table 1 C) but does not divide. P4.p and P8.p are competent but do not divide in hermaphrodites
The vulval competence group can be defined as the group of cells that can adopt a vulval fate after ablation of P(5–7).p. Both in females and hermaphrodites, P4.p and P8.p can adopt a vulval fate after laser ablation of P(5–7).p in the L1 stage (P3.p and P9.p do not adopt a vulval fate). Thus, the competence group includes P(4–8).p. P8.p seems to switch to a vulval fate more often than P4.p, at least in females (Tables 1,2 C1–2).
Strikingly, P8.p divides in females but not in hermaphrodites, whereas P4.p does not divide in either morph. The two morphs thus show a difference in the division of a cell belonging to the vulval competence group (Figs. 2B, 4C, F). Surprisingly, in females, the two cells of the vulva competence group that do not adopt vulval fates, P4.p and P8.p, show distinct division patterns (Fig. 2B).
Inductive signaling from the gonad to the vulval precursor cells differs in females versus hermaphroditesThe contribution of inductive signals from the gonad to pattern formation of Pn.p fates were studied by laser ablations of different gonadal cells at different times, as in Félix and Sternberg (1997, 1998), Sigrist and Sommer (1999), and Félix et al. (2000).
In females, ablation of the gonadal primordium shortly after hatching results in P(5–8).p adopting a non-vulval fate with one division, like P8.p in non-ablated females (Table 1 A1). By contrast, after a similar ablation in hermaphrodites, P(5–8).p do not divide in most cases (Table 2 A1). An induction of P(5–7).p division takes place in the hermaphrodite during the L1 stage (Table 2 A2; the division itself taking place in the L3 stage). In both morphs, P(5–7).p are induced to vulval fates by Z1.pp and Z4.aa or their progeny (the ventral uterine group), shortly after their birth. Because of the timing difference in gonadal divisions, vulval induction occurs in the late L1 stage in females (Table 1 A2–5) and in the late L2d stage in hermaphrodites (Table 2 A2–5). The induction of vulval versus non-vulval fates thus displays a large heterochronic shift between the two morphs.
Table 1 Cell ablations in the female morph. Ablated cells and the time of ablation are indicated in the “Ablation” and “Time” columns. The lines are lettered and numbered corresponding to the type of ablated cells and ablation times, respectively. [AC anchor cell (the anchor cell is either Z1.ppp or Z4.aaa), VU ventral uterine precursors (the three cells of the Z1.ppx/Z4.aax group that did not become the anchor cell), X ablated Pn.p cell]. “Z1.ppx + Z4.aax” in line A4 are the same cells as “AC + 3 VU” at later times, once the AC has been specified. Early L1 corresponds to the time before Pn rotation (see Sulston and Horvitz 1977); early L3 corresponds to the time of seam cell divisions (see Sulston and Horvitz 1977); mid L3 to the time after dorsal uterine precursor divisions (see Kimble and Hirsh 1979). The vulva lineage of ablated animals was scored in the L4 stage. As indicated in Fig. 2, S indicates a non-vulval fate without division of the Pn.p fate, SS indicates a non-vulval fate with one division, ssss with two divisions. Induced cells divide two to three times and their progeny form an invagination; the fate of their granddaughters is indicated by U (undivided) or T (transverse division). In some cases, the exact lineage could not be followed and Ind. indicates an induced fate and Ind.x an induced fate with x being the number of progeny. The number of invaginations is indicated in the Inv. column Table 2 Cell ablations in the hermaphrodite morph. At early timepoints of ablation during vulval fate induction, the progeny of each Pn.p cell forms a small distinct invagination. At later timepoints of ablation, the progeny of the three induced cells form a single deeper invagination (ShSp sheath and spermatheca precursors, DU dorsal uterine precursors, L3d post-dauer stage with an open mouth; other abbreviations are as in Table 1)The next step in vulval patterning is the specification of inner versus outer vulval fates. In both morphs of Rhabditis sp. SB347, induction of the inner fate occurs in P6.p daughters (Table 1 A6–8, Table 2 B2–5), as in Oscheius tipulae CEW1 (Félix and Sternberg 1997). However, the source of the signal differs between females and hermaphrodites. In hermaphrodites, ablation of the anchor cell at dauer exit results in P6.p adopting an outer UUUU lineage (Table 2 B1–2), whereas in females, the AC can be ablated in the early L3 stage without alteration in vulval lineage: ablation of the ventral uterine precursors together with the anchor cell is necessary to block induction of the primary lineage (Table 1 A5, B1). Ablation of the ventral uterine precursors alone has no effect (Table 1 B2).
In summary, in the female life-cycle, P(5–8).p are specified to divide once (non-vulval SS fate) autonomously from the gonad (at least from the time of hatching). Pn.p fate patterning then occurs in two inductive steps (Fig. 3B): (1) in the late L1 stage, vulval fates are induced in P(5–7).p by the Z1.ppx + Z4.aax group; (2) in the late L3 stage, inner vulval fates are induced in P6.p daughters by the same cells (now differentiated as AC and VU precursors. In the hermaphrodite, Pn.p fate patterning occurs in three inductive steps (Fig. 3C): (1) in the L1 stage, P(5–7).p are induced to divide once (non-vulval fate) by Z1 and Z4; (2) in the late L2d stage, they are induced to a vulval fate by the Z1.ppx + Z4.aax group; (3) in the late L3 stage, P6.p daughters are induced to an inner vulval fate by the AC.
Fig. 3A–CDifferences in vulva patterning mechanisms between C. elegans and the two morphs of Rhabditis sp. SB347. A In C. elegans, P(3–8).p are specified to be part of the competence group independently of the gonad. An induction of vulval fates by the anchor cell (AC) occurs during the L3 stage, prior to the division of the Pn.p cells. The 2°/1°/2° pattern of fates of the three induced cells may be formed through two mechanisms: (1) the anchor cell signal may act as a morphogen and (2) lateral signaling from P6.p to its neighbours inhibits the 1° fate (blue) and activates their 2° fate (red). Anterior is to the left, dorsal to the top. B In the Rhabditis sp. SB347 females, P(5–8).p are specified at hatching to divide once (SS lineage, yellow), autonomously from the gonad (it cannot be ruled out that an earlier gonadal induction of their parents occurs before hatching). A first gonadal induction step from Z1.pp and Z4.aa (and their progeny) in late L1/early L2 induces P(5–7).p from a non-vulval fate (SS lineage, yellow) to an outer vulval fate (UUUU lineage, red). A second induction step from the progeny of Z1.pp and Z4.aa, i.e. the AC and ventral uterine precursors (VU), induces the daughters of P6.p to adopt an inner vulval fate (TUUT lineage, blue). C In the Rhabditis sp. SB347 hermaphrodites, the somatic gonad precursors Z1 and Z4 induce P(5–7).p in the L1 stage to adopt an SS lineage (yellow versus grey). The second gonadal induction step occurs in late L2d/early dauer, originates from Z1.pp and Z4.aa (and their progeny) and induces P(5–7).p to an outer vulval fate (red versus yellow). A third induction step from the anchor cell induces the daughters of P6.p to adopt an inner vulval fate (blue versus red)
Fig. 4Gonad and vulva development in the female (A–C) and the hermaphrodite (D–F). Animals were photographed under Nomarski optics with a 100× objective. Anterior is to the left in all pictures, except A; dorsal is to the top. In the mid-L1 stage (when the Pn cell nuclei have just migrated along the ventral midline), the somatic gonad is much larger in females (A) than in hermaphrodites (D), and in the former, the somatic gonad precursors Z1 and Z4 have divided (only Z1.p is visible in this plane of focus). In the late L1 stage in females (B), Z1.aa (visible in this plane of focus) and Z4.pp are already born, whereas at the beginning of the hermaphrodite L2d stage, Z1 and Z4 remain undivided (E). Finally, in the L4 stage, P8.p has divided in the female (C), but not in the hermaphrodite (F). Spermatogenesis is visible in the gonad of the latter. White arrowheads point to undivided internal granddaughters of P6.p in C and F
Discussion Morph and sex determinationsHere we have described the development of alternative morphs of a rhabditid nematode in a standardized culture environment. This provides a unique convenient model system to study alternative morphs in a nematode belonging to the same family as C. elegans.
A Rhabditis species with a small proportion of females and males compared to hermaphrodites was described by Maupas (Maupas 1900) as Rhabditis viguieri, but no mention is made of a dauer stage. The ecological significance of the two morphs and of the waving behaviour of dauers remains to be clarified: this species may be associated with a tick as a carrier or parasitic host (see Materials and methods). Mechanistically, Rhabditis sp. SB347 provides a possible genetic system to study morph and sex specification in a more complex life-cycle than that of C. elegans. In the parasitic species Heterorhabditis and Strongyloides ratti, as for C. elegans dauer specification, females are committed to become infectious after hatching: proportions of the two morphs can still be altered by changing environmental conditions in young larvae (Strauch et al. 1994; Viney 1996). In Rhabditis sp. SB347, a difference in gonad size between hermaphrodites and non-hermaphrodites is already observed at hatching, suggesting that morph specification has probably occurred earlier, i.e. during embryogenesis (although we cannot rule out that it is still reversible). Coexistence of the two morphs implies that the culture conditions that were used correspond to a point in a potentially plastic response where the two morphs coexist in given proportions.
Sex determination is another puzzle when males only occur in one of two generations, as in Rhabditis sp. SB347 and many parasitic species. In the parasite Strongyloides ratti, sex determination is chromosomal (with haplo-X males as in C. elegans): parthenogenetic XX infectious females give rise to other infectious XX females, and to free-living XX females and XO males; cross-progeny of free-living females and males is female. These observations seem to imply a high rate of X chromosome non-disjunction for production of XO males, followed by a selective loss of non-X bearing sperm in the progeny of males (Harvey et al. 2000; Harvey and Viney 2001). In Heterorhabditis, use of a morphological mutant also demonstrates that male/female cross-progeny contain a very low ratio of males (actually lower than self-progeny of hermaphrodites; Dix et al. 1994).
Rhabditis sp. SB347 belongs to the family Rhabditidae and is closer to Heterorhabditis (and Caenorhabditis) than to Strongyloides (Blaxter et al. 1998; De Ley and Blaxter 2001). It also shares its hermaphroditic mode of reproduction in the dauer/infectious generation with Heterorhabditis. However, from a phylogenetic study of the family, these characters appear convergent (K. Kiontke and D. Fitch, personal communication).
Plasticity and evolution of reproductive system developmentBetween the two morphs, extensive differences are found in the developmental program of animals with the same genotype. The internal and/or external cues that direct an embryo towards one or the other morph are likely to result in the production of specific hormones, or gene expression states, that in turn influence further postembryonic development of the reproductive system.
Heterochronic changes in gonadal development have been previously described between different nematode species (Sternberg and Horvitz 1981; Félix and Sternberg 1996). In Rhabditis sp. SB347, they occur between alternative morphs in the same species: the gonad develops later when the animals go through the dauer stage. If the dauer corresponded to a stressful situation, at least in an ancestor of this species, this heterochronic change may have been selected as a temporarily reduced resource allocation to the reproductive system (the gonad has a much smaller size in the dauer compared to the L3 stage). This heterochronic change is further reflected in the timing of induction of the vulva by the gonad, which occurs in late L1 in females versus late L2 in hermaphrodites (Fig. 3B). Other differences between the two morphs cannot however be easily explained by gonadal development heterochrony, for example the difference in source of the last induction, or in P8.p lineage.
Even though C. elegans does not display morphs with distinct reproductive modes, nor extensive gonadal development heterochrony, it will be interesting to study whether its vulval development after dauer exit differs from that in the L3 stage. It is noteworthy that some Ras pathway mutations in C. elegans are partially suppressed by passage through the dauer stage (Ferguson and Horvitz 1985).
In addition to this plasticity between the two morphs, several aspects of vulva development are remarkable in Rhabditis sp. SB347, especially when compared to other Rhabditidae. First, the inner granddaughters of P6.p divide in all other studied Rhabditidae but not in Rhabditis sp. SB347. This division pattern is found in the Diplogastridae (Sommer and Sternberg 1996; Sommer 1997). Based on the morphology of its stoma and pharynx and sequence of its 18S DNA and RNA polymerase II loci, Rhabditis sp. SB347 is clearly a member of the family Rhabditidae and appears most closely related to a clade comprising Rhabditella; therefore it is not close to the Diplogastridae (K. Kiontke and D. Fitch, personal communication). The vulval division patterns of Rhabditis sp. SB347 and the Diplogastridae must therefore be convergent. A second specific feature of Rhabditis sp. SB347 within the Rhabditidae is the induction of vulval fates before anchor cell specification by a group of several ventral cells of the gonad. In C. elegans, Oscheius tipulae or Rhabditella axei, vulval fates are induced by the anchor cell in the L3 stage (Kimble 1981; Félix and Sternberg 1997). At the molecular level, the anchor cell in C. elegans is the only cell of the ventral uterus to express the LIN-3 inductive signal in the L3 stage (Hill and Sternberg 1992). Although early vulval induction by several gonadal cells was observed in other nematode families (Sigrist and Sommer 1999; Félix et al. 2000), this is the first described case in the family Rhabditidae. Another unusual feature is the induction by Z1 and Z4 of a division of P(5–7).p in the hermaphrodites, without vulval specification. Finally, the fact that both P4.p and P8.p are competent in females, but adopt different non-vulval lineages, implies the existence of two different non-vulval cell fates within the vulva competence group.
ConclusionsRhabditis sp. SB347 presents two morphs that resemble complex life-cycles of parasitic nematodes but can be studied in standard lab culture conditions. Developmental processes that are well studied in C. elegans are different between the two morphs, demonstrating phenotypic plasticity in development.
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