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Seminars in Cell & Developmental Biology 18 (2007) 362–370
Review
Evolution of the control of sexual identity in nematodes
Andre Pires-daSilva ∗
UT Arlington, Department of Biology, 501 S. Nedderman, 337 LS Building, Arlington, TX 76019, United States
Available online 19 January 2007
Abstract
Most animals are male/female species and reproduce sexually. Variation in this pattern of reproduction has arisen many times during animal
evolution, particularly in nematodes. Little is known about the evolutionary forces and constraints that influenced the origin of self-fertilization,
for instance, a type of reproduction that seems to have evolved many times in the phylum Nematoda. Caenorhabditis elegans, a very well known
nematode, provides the framework for comparative studies of sex determination. The relative ease with which nematodes can be studied in the
laboratory and the fact that many recently developed techniques can be applied to many species make them attractive for comparative research.
It is relatively poorly understood how the evolution of new types of sex determination and mode of reproduction results in changes in genome
structure, ecology and population genetics. Here, I review the evolution of sex determination and mating types in the phylum Nematoda with the
objective of providing a framework for future research.
© 2007 Elsevier Ltd. All rights reserved.
Keywords: Sex determination; Evolution; Nematodes
Contents
1.
2.
3.
4.
5.
6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Making one sex different from the other . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Chromosomal and environmental sex determination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Evolution of the sex determination pathway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Evolution of self-fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
Nematodes were one of the first animals chosen for cytological studies, which ultimately led to the discovery of the
correlation between chromosomal make up of an embryo and
its future sexual development—male or female [1]. The study
of the mechanisms and evolution of sex determination intersects
several fundamental questions in biology such as why and how
sex is maintained, what forces govern the evolution of genome
structure, how ecological factors constrain or favor reproductive
mode, and how genetic networks evolve.
∗
Tel.: +1 817 272 1383; fax: +1 817 272 2855.
E-mail address: [email protected].
1084-9521/$ – see front matter © 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.semcdb.2006.11.014
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It is estimated that there are about 500,000 nematode
species [2], most of them uncharacterized. One species of
nematode, Caenorhabditis elegans, is arguably one of the bestcharacterized metazoans. This knowledge provides a basis for
comparative studies to understand the great variation found in the
phylum. Now, with the numerous genome sequencing projects
and the possibility of applying new technologies (e.g., FISH,
microarrays and RNAi) to previously genetically intractable
organisms, there is the opportunity to expand and address questions to a higher number of nematode species.
Nematodes are particularly suited for comparative studies
because they show a rich diversity in sex determination mechanisms, have relatively small genomes, simple body plans and
live in a variety of ecological contexts. The consequences of the
evolution of androdioecy in nematodes (populations consisting
A. Pires-daSilva / Seminars in Cell & Developmental Biology 18 (2007) 362–370
363
of males and hermaphrodites), for example, are not well understood in terms of population genetics or evolution of the genome.
Importantly, many species of nematodes are plant and animal
parasites. Advances in knowledge and technology for manipulating sex ratios may open up the possibility of controlling their
reproduction.
In this review, I summarize recent developments in comparative analysis of evolution of sex determination and mating
systems in Nematoda (for more specific reviews about this subject in C. elegans and close relatives, see Refs. [3,4]). The
purpose of this review is to synthesize the variations found in
this phylum and highlight potential new avenues of research.
2. Making one sex different from the other
Most nematodes have conventional sexual reproduction, with
morphologically distinct sexes. Males and females are defined
by the size and motility of their gametes: males produce small,
motile gametes (usually in profusion), whereas females produce
larger, fewer and immotile gametes. Hermaphroditic nematodes
produce both gametes, and reproduce mainly by self-fertilization
(as opposed to the reciprocal sperm-swapping seen in other
phyla). Since nematodes reproduce mainly by internal fertilization, an entire array of signals, body structures and behaviors
evolved for mate recognition and efficient fertilization.
In nematodes, most of the sexually dimorphic characters are
restricted to the reproductive and nervous system, although differences in body size [5,6], pheromone production [7] and life
span have also been noted [8]. C. elegans, a hermaphroditic
species, has extensive sexual dimorphism (Fig. 1). It includes
all tissue types and about one third of the adult somatic cells
[9–13]. The hermaphrodites are bigger, have two gonad arms
(didelphic), a pair of organs where the sperm is stored (spermathecae), a vulva and a yolk-producing intestine [10]. Didelphic
gonads are probably ancestral for females, but males usually
have a single testis that extends anteriorly [14]. Males are slender and have various sensory and copulatory structures (i.e.,
spicules, fan, and rays) in the tail that are used to locate the
vulva and inseminate the hermaphrodite. Sex-specific muscles
and neurons are involved in egg-laying in hermaphrodites and
mating, copulation and locomotory behavior in males. In some
nematodes sexual dimorphism can be very dramatic: the Trichosomoides crassicauda male is small enough to enter the female
by way of the vulva, spending its life within the uterus [15,16].
Fig. 1. Schematic drawing showing extensive sexual dimorphism between C.
elegans hermaphrodites and males. The rays in the male contain ciliated sensory
neurons that respond to chemical and mechanical cues from the hermaphrodite.
The male uses the fan to keep the male oriented with his ventral side facing the
hermaphrodite. The spicules hold the vulva open for sperm transfer. Drawings
based on www.wormatlas.org.
About 12% of the C. elegans genes show differential transcriptional activation between males and hermaphrodites [17].
However, the differences are mostly restricted to the level of
expression and tissue-specificity rather than gender-specific
expression [18]. Only few genes are known to be specifically
transcribed in only one sex (e.g., cwp genes [19]; lov-1 and pkd-2
[20]). It is therefore likely that the extensive differences between
males and females do not arise by gender-specific genes. This
conclusion is supported by genetic analyses in which gene mutations that cause defects in males also affect hermaphrodites
[21–23]. Many of the mab genes (for male abnormal), for
instance, which have been initially isolated because of their sexspecific defects, were found to have phenotypes in both sexes
[24].
Central to sexual dimorphism is the activation of the gene
transformer-1 (tra-1) that acts as a repressor of male genes in the
hermaphrodite and as an activator in the male. This gene, which
codes for a zinc-finger transcription factor, regulates about 364
genes in the soma of C. elegans males and hermaphrodites [18].
Most phenotypic sexual differentiation occurs postembryonically [12], and tra-1 seems to act no earlier than the first larval
stage for most cell fate decisions [25,26].
To date, only two genes, egl-1 and mab-3, have been identified as direct target genes of TRA-1 in the soma (Fig. 2). egl-1
Fig. 2. Model for sex determination in C. elegans. Proteins in blue are the core components of the pathway that control sex determination in the soma and in germline,
while the ones in red are involved only in the germline sex determination. Proteins upstream of HER-1 also control dosage compensation. The line connecting TRA-1
and TRA-2 represent a physical interaction. For more details, see text and reference [4].
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A. Pires-daSilva / Seminars in Cell & Developmental Biology 18 (2007) 362–370
and mab-3 control a subset of sex-specific events in C. elegans,
such as the survival of hermaphroditic-specific neurons [27],
yolk production in the intestine of the hermaphrodite [28], and
expression of a male-specific cell lineage [29].
3. Chromosomal and environmental sex determination
Most nematodes have chromosomal sex determination, in
which the female is XX and the male is heterogametic sex (XY)
or XO (the O indicates the absence of Y). It is likely that the
XX:XO sex determination system is ancestral because it is found
in most of the nematode clades so far studied (Fig. 3). The few
XY systems occur among parasitic nematodes of clades I, III and
IV (following the nomenclature of Ref. [30]). It is thus possible
that the XY system is derived from the fusion of an autosome to
the old X-chromosome [31], although clear cytogenetic evidence
is still lacking.
Gonochoristic, i.e., male/female, nematode species with
a chromosomal sex determination usually have a sex ratio
of 1:1 (although exceptions are known, e.g., Ref. [32]). In
hermaphroditic nematodes, however, males are rare. For example, when C. elegans is maintained in laboratory conditions,
only 0.05–0.3% of the population is male [33,34]. In this nematode, the frequency of XX hermaphrodites and XO males is
primarily driven by two factors: (1) the ability of male sperm to
outcompete the sperm of the hermaphrodite [35]; (2) the rate of
random sex chromosome non-disjunction during spermatogenesis in the hermaphrodite [36]. Normally, each hermaphrodite
gamete contains one sex chromosome. However, rare chromosomal non-disjunction events lead to the production of gametes that
lack an X chromosome, which then fertilize X-bearing gamete,
resulting in the formation of male (XO) zygotes [37].
The molecular basis for the XX:XO sex determination system is best understood in the rhabditid C. elegans (for reviews,
see Refs. [38,39]). Sex determination in C. elegans is based
on a chromosome-counting mechanism that is achieved by a
set of autosomal signal element genes (sea-1 and others) that
oppose X signal element genes (sex-1, fox-1 and others) [40,41].
As a result, the sex-determining gene xol-1 is repressed in
XX animals, thereby promoting the female fate [42–46]. xol1 repression is the first event in a cascade of genetic interactions
that results in the activation of tra-1, the most downstream global
regulator of sex determination (Fig. 2).
It is well established that in other phyla the molecular
and genetic mechanisms underlying sex determination can be
completely distinct, even when comparisons of closely related
species are undertaken [47,48]. The most striking differences are
in the more upstream events of the sex determination pathway.
Intriguingly, the ortholog of the C. elegans X signal element fox1 is also in chromosome X of the distantly related nematode P.
Fig. 3. Diversity of somatic and germline sex determination in nematodes. Gonochorism and XX:XO are the most common mating types and sex determination
strategies, respectively. In this phylogenetic tree, deviations from the common types of somatic and germline sex determination are highlighted; environmental sex
determination and chromosomal sex determination type XX:XY have evolved independently in almost all clades. The evolution of species capable of producing
oocytes and sperm by the same individual also evolved multiple times (asterisks). References: H. contortus [129]; C. elegans [97]; H. bacteriophora [130,131]; P.
pacificus [132]; S. ratti [133]; R. buffonis [53]; Panagrolaimus sp. (PS1732) [134]; S. carpocapsae [135]; S. hermaphroditum [136]; A. avenae [137]; Acrobeloides
sp (PS1146) [134]; S. celeris [118]; M. hapla [119]; T. alatus [138]; B. malayi [139]; H. spumosa [140]; A. lumbricoides [141]; C. incurvum [50]; P. allius [142]; T.
spiralis [143]; T. muris [144]; X. attorodorum [145]; M. nigrescens [64]; C. papillatus [146].
A. Pires-daSilva / Seminars in Cell & Developmental Biology 18 (2007) 362–370
pacificus (Pires-daSilva, pers. obs.). Functional analysis of this
gene and other signal element gene orthologs will be necessary
to test if the counting mechanism is the same between these
nematodes.
Ascarids are especially rich in sex chromosome karyotype
variation: spermatocytes of Toxocara canis and T. cati contain 2
X chromosomes, males of Baylisascaris transfuga have 3 X and
1 Y chromosome [49], and Contracaecum incurvum (Ascaris
incurva) males have a single Y chromosome that pairs with 8
X chromosomes, while the females have 16 X chromosomes
[50] (Fig. 3). The exact mechanism by which the multiple sex
chromosome determination system evolved is not clear, but similar systems are also found in other groups of animals, such as
insects, ostracods and the platypus [51,52].
Nothing is known about the molecular switch mechanism
present in XX:XY species. One possibility is that it is based on a
genic balance mechanism, which depends on a balance between
female-determining genes in the X chromosome and male determining genes in autosomes, as with C. elegans. Another option
is that the Y chromosome plays a dominant role in the determination of sex, similar to the situation in humans.
Some nematodes alternate between different types of sex
determination in their life cycle, having XX:XO sexes in one
generation and XX-only animals in the other. How can XO
males, which produces two kinds of sperm (half with the
sex chromosome and the other half without it), generate only
XX animals in the following generation? In the nematode
Rhabdias bufonis (synonyms: Angiostomum nigrovenosum or
Rhabdonema n.) it seems that the male X-bearing sperm have
precedence for fertilization. Hence, the resulting progeny will
be largely XX hermaphrodites rather than equal proportions of
XX and XO [53–55]. Sperm precedence for X-bearing sperm
cells has been also described for other nematode species [56].
Spermatogenesis in the ovotestis of the XX hermaphrodite follows a different course of that from males in order to generate
XX females and XO males in the following generation: all the
sperm contain an X at first but in half of them it is extruded and
lost at the time when the developing sperm separates from its
residual cytoplasm. Thus, the XX hermaphrodites produce one
kind of oocyte but two kinds of sperm cells. When these sperm
cells fertilize oocytes, XX and XO individuals of the sexual generation are produced once again. A more recent study reports the
same kind of X-chromosome loss in a related species [57].
Oxyurids (clade III), also known as pinworms, are the only
group of nematodes known to determine their sex with a haplodiploid system [58]. In this type of sex determination, males
are haploid and develop from unfertilized eggs, whereas females
are diploids and derive from fertilized eggs. One possible mechanism by which sex determination might be regulated is via
chromosome dosage as occurs in C. elegans. Alternatively, a
highly polymorphic X chromosome locus might control the sexual fate, in a similar way as occurs in honeybees [59]. In these
insects the sex determination locus, when heterozygous, induces
female development and when hemizygous the eggs develop into
males. Additional mechanisms are possible (e.g., Ref. [60]), but
testing of the different possibilities will be only possible when
genetic analyses are applied.
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Environmental sex determination evolved independently in
various nematode clades [61,62] (Fig. 3). For the parasitic
mermithid nematodes (e.g., Mermis nigrescens), the degree of
infestation, the size of the host and the sex of the parasite which
first penetrated the host seem to be important factors [63,64]. For
the tylenchid Meloydogine incognita sex determination depends
on conditions of feeding: when favorable the eggs develop into
females and when not favorable they become males [65]. In
Meloidodera floridensis, larvae subjected to starvation by keeping them in tap water for four months resulted in large proportion
of males [66]. In Diplenteron colobocercus (syn. Mononchoides
potohikus) the induction of males seems to be mediated by a
pheromone-like substance [67].
Nematodes with environmental sex determination have a high
rate of intersexes [65]. Intersexes are usually functional females
(i.e., individuals with well developed reproductive system that
produces oocytes) with some male somatic characters such as
spicules [68]. In M. javanica and M. incognita, female larvae
can undergo sex reversal relatively late in development, which
causes the appearance of males with two gonadal arms (typical of
females) instead of one [65]. Sex reversal and intersexes can be
induced experimentally in crosses between two different species,
such as in the rhabditids C. remanei and C. briggsae [69]. In
this case, the effect has been attributed to dysgenic interactions
among fast-evolving sex determination genes.
The existence of all this diversity in sex determination systems raises many questions about what selective forces underlie
their evolution and how one system evolves into another.
Hodgkin [70] demonstrated that by using combinations of different C. elegans sex determination mutant strains it is possible
to mimic many types of sex determination systems, including
environmental sex determination and multiple X and Y chromosomes. These results suggest that a few mutational events
can radically change the sex determination system.
4. Evolution of the sex determination pathway
The sex determination pathway that leads to the regulation
of TRA-1 has been very well characterized at the genetic and
molecular level in C. elegans [38]. Chromosomal signals are
translated into a set of genetic interactions that result in the sexspecific activation of a signal transducing pathway mediated by
HER-1 (Fig. 2). HER-1, a male-specific protein [71], is a small
secreted ligand that binds to the TRA-2 membrane receptor on
the cell that secretes it, or on neighboring cells [72,73]. In a
final step, TRA-2 regulates TRA-1 via three FEM proteins by
unknown mechanisms.
Some components and dynamics of the sex determination
pathway show resemblance in at least three aspects when compared to hedgehog (hh) signalling, a pathway involved in various
developmental processes in vertebrates and invertebrates [74].
First, the membrane receptor of Hh, Patched, is structurally similar to TRA-2 [75,76]. It is important to note, however, that Hh
and HER-1 show no sequence or protein fold similarity and
thus are not likely to be related by descent. Second, TRA-1 is a
homolog of Drosophila cubitus interrruptus (Ci), the transcription factor of the hh signalling pathway [77]. Third, TRA-1 is
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post-trancriptionally regulated by proteolytic cleavage, like Ci
[78,79]. These similarities suggest that the hh signalling pathway
has been co-opted for sex determination in C. elegans [80].
As an alternative hypothesis, it has been suggested that the
sex determination pathway arose in sequential steps, rather
than being recruited from an already existent pathway. According to Wilkins [81], mutations in sex determination genes that
cause a detrimental sex ratio are countered by the acquisition of
modifiers into the pathway. These modifier genes would then reestablish the optimal sex ratio for a given population. Mutations
that cause a production of excess of females in the population,
for example, would be countered by the recruitment of malepromoting genes that can inhibit the female promoting factor
TRA-1. The prediction for such a scenario is that the global
sexual regulator TRA-1 is the most ancient part of the sex determination cascade, and the genes upstream of it are sequentially
younger acquisitions of the pathway.
These hypotheses can be tested by comparing the sex determination between different nematode species. So far, no additional
components of the hh signalling pathway have been found in
nematodes, such as Hh, Hedgehog-interacting protein (Hip) and
Smoothened (Smo) [80,82]. It is therefore not clear whether the
entire pathway was present in the lineage that gave rise to the
nematodes or in which nematode clade this pathway might has
been recruited for sex determination. With the various genome
projects underway, it is possible that these homologs will still
be identified in nematodes.
Although the sex determination gene sequences are known
to evolve rapidly [83–85], functional tests suggest that the pathway is essentially conserved within the Caenorhabditis genus
[86,87,3]. In the diplogasterid Pristionchus pacificus, a more
distantly related nematode, many of the C. elegans sex determination gene homologs have been found (A. Pires da Silva,
unpublished data). Their role, however, has been uncovered for
only one of these genes, tra-1. P. pacificus tra-1 (Ppa-tra-1) lossof-function mutants show the same sex reversal phenotype as
Cel-tra-1, suggesting that the function of this gene is conserved
between C. elegans and P. pacificus [88].
It is still not clear whether the direct regulation of C. elegans tra-1 targets, mab-3 and egl-1, is conserved in P. pacificus.
mab-3 is member of a family of transcription factors that contain a DM domain [89]. This domain is also present in a
male-promoting transcription factor, Doublesex (DSXM ), the
most downstream regulator of sex determination in the fruitfly
Drosophila melanogaster. The similarity in biological functions
between DSXM and mab-3 suggests that a component of the
sex-determination mechanism is shared between different phyla.
Additional DM family members have been implicated in various
roles in sexual development for C. elegans [90], mouse [91] and
fish [92]. However, neither the regulation of these genes, nor
the targets show significant conservation across phyla [93]. It is
therefore possible that the recruitment of DM-domain factors for
male-specific function in development occurred multiple times
as result of convergent evolution.
In summary, more comparative studies between nematodes
may shed light on to the evolution of sex determination. With
the recent development of sophisticated genetic and molecular
tools for P. pacificus, traditional forward genetics approaches
can be applied to this nematode [94,95,88]. Together with the
availability of the genome sequence, forward genetic screens
can be complemented with reverse genetic approaches to test
whether C. elegans homologs have conserved functions in other
species.
5. Evolution of self-fertilization
Many nematodes are capable of autotokous reproduction,
which is the production of progeny by a single parent. This mode
of reproduction includes hermaphroditism and parthenogenesis,
in which progeny develop from fertilized and unfertilized eggs,
respectively. Hermaphroditism in nematodes is characterized by
the production of sperm and oocytes by the same individual.
Only rarely will the male – as characterized by the presence of
spicules and absence of vulva – produce both types of germ cells
[96]. Typically, the external morphology of hermaphrodites is
morphologically identical to females of closely related gonochoristic species [97]. Hermaphroditic nematodes probably evolved
from gonochoristic animals and therefore represent a derived
condition [98].
In most hermaphroditic nematodes a single organ, the
ovotestis, produces both oocytes and sperm. There are about
17/460 rhabditid species with an ovotestis, scattered in 11 out of
a total of 44 genera [2,99,100]. The presence of an ovotestis has
been also found in parthenogenetic species, where the sperm
serve as an activator of embryogenesis but do not contribute
genetic material to the next generation [101–104]. At least 5/17
species with ovotestis have been confirmed to self-fertilize and
produce zygotes by pronuclei fusion, which meet the criteria for
being hermaphroditic: C. elegans, C. briggsae, Oscheius tipulae
CEW1, P. pacificus and H. bacteriophora. Phylogenetic analysis
indicates that the most parsimonious interpretation for the evolution of hermaphroditism is that it evolved several times within
the eurhabditids [99] and diplogasterids [100].
General features of germline development are conserved
between different groups of nematodes. However, the role of the
somatic gonad in the regulation of spermatogenesis and the timing of spermatogenesis seems to vary [35,105]. In C. elegans,
spermatogenesis and oogenesis do not occur simultaneously:
the gonad produces several hundred sperm during the last larval
stage and then switches to oocyte production as adults. At the
distal part of the ovotestis, the germ cells are mitotic and serve
as stem cells. Although germline and somatic sex determination
proceed by a similar genetic pathway [38], they differ in two
aspects. First, the brief production of sperm in the last larval
stage is independent of the X chromosome to autosome ratio.
Second, there are additional genes in germline sex determination that have no role in somatic sex determination (i.e., the fog
and mog genes).
The genetic basis for germline sex determination has been
well characterized in C. elegans [106]. fog-2, the most upstream
germline sex-specific regulator, codes for a cytoplasmic protein
of the F-box family [107], and is required for spermatogenesis only in XX hermaphrodites but not in XO males. Together
with the RNA-binding protein GLD-1, FOG-2 down-regulates
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tra-2 mRNA translation, resulting in the production of sperm
[107].
Phylogenetic analyses suggest that hermaphroditism in C.
elegans and C. briggsae has occurred due to an evolutionary
convergence rather than being homologous. This conclusion is
supported by genetic data, which indicate that there are fundamental differences in spermatogenesis between these two
species. fog-2, the most upstream germline-specific regulator
of spermatogenesis in C. elegans hermaphrodites [108], is not
present in the C. briggsae genome [109]. Furthermore, other
genes involved in C. elegans hermaphroditic spermatogenesis
(e.g., gld-1, fem-2 and fem-3) do not have a function in sperm
formation in C. briggase hermaphrodites [109,86,110]. Traditional forward genetic approaches will be necessary to unravel
the genes involved in germline sex determination in C. briggsae
[4,111].
Sperm size and spermiogenesis in hermaphrodites show at
least two differences relative to males of the same species.
First, male-derived sperm are substantially bigger than hermaphrodite-derived sperm [112,113]. Second, spermiogenesis
seems to be sex-specific: mutant screens for C. elegans spermatogenesis defects have uncovered genes with hermaphroditespecific [114–116] or male-specific defects [117]. This raises
the question of how the convergent evolution of spermiogenesis
in hermaphrodites has been reflected at the molecular level.
Hermaphroditism outside of clade V is based solely on morphological criteria (Fig. 3). Studies of the aphelenchids Seinura
oxura and S. steineri showed that the gonads of these species
can produce oocytes and sperm (syngonic hermaphroditism),
and that egg production stops when the supply of sperm cells is
exhausted [118]. This mode of reproduction suggests that it is
similar to C. elegans, where the gonad produces first sperm and
then switches to oogenesis. In other nematode species, however,
spermatogenesis and oogenesis seem to occur simultaneously
[57,119], or in alternation [53,120]. The production of sperm
and oocytes in two different gonads of the same animal (digonic
hermaphroditism) has been suggested for Clarkus (Mononchulus) ventralis and Helicothylenchus digonicus [121]. For C.
ventralis, Cobb [122] describes females with one anterior gonad
that produces oocytes and a small posterior testis that produces
sperm. More detailed analysis of H. digonicus, however, failed
to confirm hermaphroditism in this species: the large spherical
structure that projects dorsally from the oviduct female gonad
that has been regarded as sperm-producing organ does not contain sperm [123]. It is clear that more detailed cytological and
genetic studies are necessary to evaluate to confirm that there
are hermaphroditic species in many nematode clades.
367
other animals, nematodes that reproduce mainly asexually are
one of the most ubiquitous plant parasites in the world [124]. To
understand the factors that are driving the evolution of sex determination and asexual reproduction, integration of many diverse
fields such as ecology, genetics and cell biology will be required.
Furthermore, basic questions such as whether there is the occurrence of hermaphroditism in non-rhabditid nematodes are still
unanswered.
The evolution of self-fertile hermaphroditism appears to be
associated with an adaptation to low effective population density, which can be caused either by low absolute numbers or low
mobility [125,126]. This mode of reproduction is of advantage
for organisms that pioneer new environments, because it assures
the production of progeny in the absence of a mating partner.
This advantage, however, comes at the cost of an increase in
the level of inbreeding. The discussion of the interplay between
factors that favor or hinder self-fertilization is beyond the scope
of this review, but much research is needed in this area. No significant correlation has been found between the ecological niche
of autotokous nematodes and their gonochoristic relatives [2];
sometimes sister species with different reproductive modes are
found in the same habitat [127]. More details about life history
characteristics are needed to better understand the variables that
influence fitness, and therefore the selective factors acting on the
reproductive mode.
Sex determination is known to evolve fast in various phyla.
However, it is not clear how exactly the sex determination
pathway evolves: does it evolve from bottom up [81]? Was the
C. elegans pathway recruited from hh signaling pathway? Were
DM-domain containing genes recruited independently in various phyla for a role in sex determination? With the development
of unbiased, forward genetic methods in various nematodes
species, the comparison of the evolution of sex determination
will be addressed at various phylogenetic scales [86,88]. Furthermore, with the various nematode EST and genome sequence
projects (e.g., http://www.sanger.ac.uk/Projects/Helminths/,
http://www.nematodes.org/nematodeESTs/nembase.html),
candidate genes can be readily identified and investigated using
reverse genetics methods, e.g., RNAi, in non-rhabditid species
[128].
Acknowledgments
I want to thank Ellen Pritham, Lenore Price and Ralf Sommer for critically reading the manuscript, and Zach Jacquays for
drawing Fig. 1. Andre Pires da Silva is funded by NSF grant
IOB#0615996.
6. Perspectives
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