Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2018 Oct;210(2):397-433.
doi: 10.1534/genetics.118.300243.

From "The Worm" to "The Worms" and Back Again: The Evolutionary Developmental Biology of Nematodes

Affiliations
Free PMC article
Review

From "The Worm" to "The Worms" and Back Again: The Evolutionary Developmental Biology of Nematodes

Eric S Haag et al. Genetics. .
Free PMC article

Abstract

Since the earliest days of research on nematodes, scientists have noted the developmental and morphological variation that exists within and between species. As various cellular and developmental processes were revealed through intense focus on Caenorhabditis elegans, these comparative studies have expanded. Within the genus Caenorhabditis, they include characterization of intraspecific polymorphisms and comparisons of distinct species, all generally amenable to the same laboratory culture methods and supported by robust genomic and experimental tools. The C. elegans paradigm has also motivated studies with more distantly related nematodes and animals. Combined with improved phylogenies, this work has led to important insights about the evolution of nematode development. First, while many aspects of C. elegans development are representative of Caenorhabditis, and of terrestrial nematodes more generally, others vary in ways both obvious and cryptic. Second, the system has revealed several clear examples of developmental flexibility in achieving a particular trait. This includes developmental system drift, in which the developmental control of homologous traits has diverged in different lineages, and cases of convergent evolution. Overall, the wealth of information and experimental techniques developed in C. elegans is being leveraged to make nematodes a powerful system for evolutionary cellular and developmental biology.

Keywords: C. elegans; WormBook; connectome; developmental systems drift; embryo; evolution; gene regulatory network; sex determination; sperm; vulva.

Figures

Figure 1
Figure 1
Phylogenies of phylum Nematoda, suborder Rhabditina, and genus Caenorhabditis, based on molecular data. (A) Inset shows the phylogenetic position of Nematoda within a very simplified phylogeny of bilaterian animals. Recent molecular studies place Nematoda together with its sister group Nematomorpha as the closest relatives of Panarthopoda (Arthropoda, Onychophora, Tardigrada) in a clade often called Ecdysozoa (Giribet 2016; Giribet and Edgecombe 2017). The phylogeny of Nematoda has been derived mainly from ribosomal RNA (rRNA) genes and contains several well-defined clades: clades I–V (De Ley and Blaxter 2004; De Ley 2006) designated in like-colored roman numerals, taxon names, and polygons; and clades 1–12 designated in black superscripts to corresponding taxon names (Holterman et al. 2008; van Megen et al. 2009). Some taxa have been left out here for simplicity. Taxa other than Rhabditina that are mentioned in this review are listed at the right. Adapted with permission from Blaxter (2011) and Kiontke and Fitch (2013). Taxa in quotation marks are paraphyletic: “Rhabditomorpha” includes all Rhabditina except Diplogasteromorpha and Bunonematomorpha. (B) Phylogeny of Rhabditina (clade V), almost entirely based on molecular data from rRNA and other loci (Kiontke et al. 2007; Ross et al. 2010; Kanzaki et al. 2017). Thickness of the lineages, as indicated in the key at lower right, indicates the approximate level of confidence estimated from statistical tests. The systematics of “Rhabditidae” was recently revised (Sudhaus 2011) based almost entirely on the molecular phylogeny (Kiontke et al. 2007) with some consideration of morphological characters to place taxa only known from literature descriptions (brown lineages). A few, mostly monotypic taxa of uncertain position are not shown. Four named suprageneric clades are shown with brackets. Despite being paraphyletic, “Rhabditidae” is a useful taxon because it includes many free-living (rarely parasitic) species with fairly similar Bauplan and excludes three specialized parasitic taxa (Angiostomatidae/Agfa, Strongylida, Rhabdiasidae) and Diplogastridae, a clade of species morphologically distinguished from “Rhabditidae” that have undergone an extensive adaptive radiation. Pristionchus pacificus and its relatives are included in the Diplogastridae. The “Rhabditidae” sister taxa to each of these special groups provide important resources for investigating the evolutionary origins of parasitism and other specializations that have resulted in adaptive radiations. Colored fonts indicate taxa in which reproductive mode has evolved from gonochorism to hermaphroditism, heterogonism or parthenogenesis (see key at lower right). Taxon names in bold font are at higher levels than the genera otherwise depicted. For more complete information, see RhabditinaDB at rhabditina.org. (C) Phylogeny for some Caenorhabditis species as inferred by molecular data from rRNA and several other loci (Kiontke et al. 2011). Due to the rapid rate of discovery, species are provisionally designated with numbers (sp. n) until names can be attached to these species units (Félix et al. 2014). Only 28 of the ∼50 known species are shown here; however, this phylogeny shows all the major known clades (demarcated here as “species groups”). Several Caenorhabditis species are only known from morphological descriptions and not included here. Hermaphroditic species are indicated in red font; other species are gonochoristic.
Figure 2
Figure 2
First embryonic cell divisions in C. elegans and variations in other species. Top panel (A–F) schematic representation of the two first cell division of the C. elegans embryo. Microtubules are shown in green, centrosomes are represented by black dots and nuclei by white circles. Polarity proteins are shown in gray and yellow. (A) Initially, the oocyte is unpolarized. After the sperm entry (on the right), female meiosis resumes (spindle on the left). (B) After fertilization, polarity proteins are asymmetrically localized and the sperm entry site defines the posterior pole of the cell on the right (B). In response to polarity, the mitotic spindle (D) and cell fate determinants (E) are asymmetrically localized. During the second cell division, spindle orientation is different between the two cells (E), giving rise to a rhomboid organization of blastomeres at the four-cell stage (F). At this stage, the P2 cell sends a Wnt signal to EMS. Phenotypic changes: timing of cell divisions and cell orientations can vary between species leading to different cellular contacts and blastomeres organization. Cryptic changes: among species that have similar embryonic cell divisions than C. elegans, evolutionary changes are found in the polarization of the embryo, the positioning of the first mitotic spindle or in cell/cell communication.
Figure 3
Figure 3
Convergent evolution of self-fertility via distinct changes alterations of germline sex determination. The core body-wide sex determination pathway (black), which acts in all dimorphic tissues, is shared with outcrossing relatives (top). Upstream factors that sense X dosage and regulate both sex determination and dosage compensation (xol-1 and the sdc genes), are not depicted here for simplicity. The XX hermaphrodites of C. elegans (middle) and C. briggsae (bottom) both produce sperm in an otherwise female body by germline-specific modification of sex determination. Germline-specific factors that promote sperm production in each are indicated in green, while those limiting it are in red. Note that in the C. briggsae case, the influence of she-1 on tra-2 is indirect, and the action of the pathway consisting of puf-2, puf-1.2, gld-1, and puf-8 has not yet been placed along the global pathway, and is thus conservatively depicted as a parallel pathway. Pleiotropic accessory factors with important roles in sexual fate are indicated in gray. The alternative functions of homologous genes and the role of species-specific genes in both hermaphrodites are particularly noteworthy. The arrows connecting fem genes directly to sperm fate in C. elegans depicts how loss of any of the fem genes phenotypically feminizes tra-1 germ cells without loss of fog-3 expression (Chen and Ellis 2000). In C. briggsae, a similar result is found for fem-3, but not fem-2, and the effect is to convert the mostly male tra-1 germ line to a consistent hermaphroditic (rather than female) pattern (Hill and Haag 2009). For this reason, the equivalent arrow is dashed.
Figure 4
Figure 4
Scenario for the evolution of self-fertility in Caenorhabditis. (A) In the gonochoristic/dioecious Caenorhabditis ancestor, males (top) store gametes as inactive spermatids in the seminal vesicle, maintained in this state by the protease inhibitor SWM-1. Upon mating and ejaculation, male spermatids (gray) pass through the glandular vas deferens, where they encounter active TRY-5 protease and the signal for the spe-8 pathway, which may be zinc ions. Once inside the female (bottom), they are activated and migrate from the uterus to the spermatheca, where they await ovulation and a chance to fertilize an egg. (B) A hypothetical first step to self-fertility is a change in germline sex determination that allows the production of some self-spermatids (light circles). These cannot activate on their own, but, after mating and transfer of some male seminal fluid, they are activated in trans (light spermatozoa). (C) In the second step, hermaphrodites evolve the ability to activate self-spermatids autonomously, by increasing the level of active TRY-5 protease (as in C. tropicalis) or the signal for the spe-8 pathway (in C. elegans and C. briggsae).
Figure 5
Figure 5
Variations in vulval development in Caenorhabditis, Pristionchus, and Auanema. Left panel: schematic representation of vulva development in C. elegans, and some cryptic variations found within Caenorhabditis. From ventral epidermal cells, six competent cells, P3.p to P8.p are defined in C. elegans. During the L3 larval stage, VPCs are specified and induced by the combined action of a graded EGF signal from the anchor cell (AC), a lateral Notch signal between the most central cells and a Wnt gradient emanating from the posterior of the body (gray wedge). Blue cells adopt a primary fate and divide to form the center of the vulva in late L4. Red cells have a secondary fate and form the lateral part of the vulva. Yellow cells form the vulva only if blue or red cells are absent. The respective contributions of the EGF and Notch pathways vary quantitatively (shown by arrows of different size) among Caenorhabditis species and even among strains of the same species. In C. briggsae, reduction in Wnt signaling (compared to C. elegans) is responsible for the lack of competency of P3.p. This could be due to truncation of the Wnt gradient (depicted here), or because of reduced sensitivity of P3.p to an identical gradient. Middle panel: Schematic representation of vulva development in P. pacificus, and variations found within Pristionchus. In P. pacificus, the VPCs are induced by redundant Wnt signaling signals sent by the gonad and the AC. The M cell, as well as the P8.p cell (which is only partially competent), send lateral inhibitory signals to prevent the adoption of 1° Cell fate by P5.p and P7.p. Within Pristionchus, cryptic quantitative changes in the signaling pathways are observed. In particular, the extent of lateral inhibition by P8.p varies frequently between and within species. Right panel: example of changes in vulva development between morphs of the same species is shown for Auanema rhodensis SB347. In this species, three sexes coexist because female larvae that go through the dauer stage become self-fertile hermaphrodite adults. This plasticity is accompanied by changes in vulva formation between females and hermaphrodites, in the number of inductive signaling steps from the gonad that are required to specify the Pn.p cells, as well as in the number of divisions of P8.p.
Figure 6
Figure 6
Male tail development in C. elegans and male tails of some other species. Top left: the left-side cell lineages giving rise to the Rn.p “tail seam” hypodermal cell, the three cells of each ray rn (with designations v1–v7, ad and pd used for comparing ray homologs across species), and the phasmid socket cells (see text). These lineages are produced from bilateral pairs of V5, V6 and T blast cells, shown in the L1 larva (Sulston et al. 1980). Red lines represent apical boundaries of cells as would be visualized by immunostaining with MH27 or AJM-1::GFP. Inset: canonical ray sublineage in which an Rn neuroblast produces an Rn.p hypodermal cell (part of the “tail seam”), two ray neurons RnA and RnB, a ray structural cell Rnst and a programmed cell death (“x”). Below the cell lineage: arrangements of these cells in the left lateral hypodermis right after their origins at early L4, and at mid-L4 after the RnA and RnB neurons have sunk a little below the surface. Tail tip cells hyp(8–11) and phasmid socket are also depicted. At the mid-L4 stage, the tail tip cells fuse and some of the Rn.p cells fuse together (leading to absence of adherens junctions separating those cells) and begin to change shape (Fitch and Emmons 1995). DIC photomicrographs at the right: tail morphogenesis, left side view. The first visual sign of morphogenesis occurs when the tail tip cells separate from the pointed L4 cuticle, round up and retract anteriorly at mid-L4. At late L4, because the tips of the rays are attached to the adult outer cuticle (beneath the L4 cuticle), the rays are formed as the rest of the body retracts and the fan folds flat around them. The fully formed adult emerges after the pointed-tailed L4 cuticle is molted off. These events do not occur in hermaphrodites/females, which retain the pointed shape of the larval tails. Bottom: left side views of adult male tails of C. elegans and four other species: Pelodera strongyloides, Metarhabditis blumi, Rhabditella axei, and Panagrellus redivivus. Outlines of the body and fan (if any) are depicted as gray lines, the internal left spicule (or fused left-right spicule in P. strongyloides) and gubernaculum are in brown, and the rays are outlined in black and labeled using the ray homolog designations. Also shown is the position of the phasmid. The tail tip cells retract to make the independently evolved peloderan tails of C. elegans and P. strongyloides, and do not retract in R. axei and M. blumi (derived, “apomorphic” leptoderan) and P. redivivus (ancestrally, “plesiomorphic” leptoderan) (see references cited in text).

Similar articles

See all similar articles

Cited by 6 articles

See all "Cited by" articles

References

    1. Aboobaker A. A., Blaxter M. L., 2003. Hox gene loss during dynamic evolution of the nematode cluster. Curr. Biol. 13: 37–40. 10.1016/S0960-9822(02)01399-4 - DOI - PubMed
    1. Albert P. S., Brown S. J., Riddle D. L., 1981. Sensory control of dauer larva formation in Caenorhabditis elegans. J. Comp. Neurol. 198: 435–451. 10.1002/cne.901980305 - DOI - PubMed
    1. Albertson D. G., Nwaorgu O. C., Sulston J. E., 1979. Chromatin diminution and a chromosomal mechanism of sexual differentiation in Strongyloides papillosus. Chromosoma 75: 75–87. 10.1007/BF00330626 - DOI - PubMed
    1. Andersen E. C., Bloom J. S., Gerke J. P., Kruglyak L., 2014. A variant in the neuropeptide receptor npr-1 is a major determinant of Caenorhabditis elegans growth and physiology. PLoS Genet. 10: e1004156 (erratum: PLoS Genet. 10: e1004316) 10.1371/journal.pgen.1004156 - DOI - PMC - PubMed
    1. Andrássy I., 1983. A Taxonomic Review of the Suborder Rha bditina (Nematoda: Secernentia). L’Office de la Recherche Scientifique et Technique Outre-Mer, Paris.

MeSH terms

LinkOut - more resources

Feedback