Weird Worms and The Tree of Life: The Relationship of Gastrotricha to Other Metazoan Phyla
by Madalyn Zimbric
BIOL/WATER 361, Fall 2012
The animal world is a diverse one; approximately 35 living phyla of animals are currently recognized, each representing a unique general body plan. Some of these are familiar and well studied, like mollusks, arthropods, and chordates, but others are more obscure. These “lesser known groups” are usually tiny, rare, difficult to study, and have no obvious economic impact, but in order to understand completely how animals are related to each other and how they evolved we must understand even minor phyla (Schmidt-Rhaesa, 2002). Gastrotricha is one of these groups of poorly understood organisms and their relationship to other metazoans is uncertain. Several hypotheses have been advanced, but the most current evidence suggests that they are nested somewhere in a group called Platyzoa.
Before we examine gastrotrichs’ relationships with other animals, let us meet the stars of this story. Gastrotrichs are minute worm-like animals less than 1 mm long that live in sediments or on surfaces in aquatic environments. Their bodies resemble elongated bowling pins with a forked posterior end and a flattened ventral side. Their surface is covered with a complex cuticle, which may be adorned with a diverse variety of plates, spines, and processes. They exhibit a rapid, gliding motion, achieved by waving cilia on their ventral surface. These cilia give the group their name, which translates as “hairy belly” (Smith, 2009). Marine species are generally simultaneous hermaphrodites and freshwater species are generally parthenogenetic. Little is known about them even in comparison to other meiofauna – the tiny animals associated with the floors of bodies of water – and very few workers specialize in studying them. Despite this lack of knowledge, it is clear that the group is monophyletic (Schmidt-Rhaesa, 2002). Some work has been done on their phylogenetic relationships and gastrotrich representatives have been included in several large phylogenetic analyses.
In the early 2000s, Gastrotricha was hypothesized to be the sister group to Ecdysozoa, a clade of animals that molt a cuticle. Familiar ecdysozoans include arthropods and nematodes. While gastrotrichs do have a cuticle, they do not molt and they have not lost locomotory cilia like the ecdysozoans have. Gastrotrichs share many morphological features with ecdysozoans, including a circumpharyngeal brain, a cylindrical, cuticularized pharynx, and a multilayer cuticle. Thus phylogenetic analyses based on morphology supported the group Ecdysozoa + Gastrotricha (Zrzavy, 2002). If this grouping were correct, it would have intriguing implications for ecdysozoan evolution. For example, the fact that gastrotrichs have both locomotory cilia and a cuticle would imply that ecdysozoans developed a cuticle before losing cilia and developing alternative locomotory structures (Zrzavy, 2002). However, the apparent homologies of the brain and pharynx may be red herrings; the brain of gastrotrichs is composed of a few commissures rather than an equi-diameter ring of neural tissue and similar pharynxes to those of gastrotrichs are found in rotifers (Edgecombe, 2011). As compelling as the grouping based on morphology may be, when molecular characters are analyzed Gastrotricha rarely nests next to Ecdysozoa.
A better supported hypothesis, borne out by several phylogenetic analyses of molecular characters, places Gastrotricha within Spiralia. The metazoans in this clade typically exhibit spiral cleavage as embryos and it includes Mollusca, Annelida, Platyhelminthes and several smaller phyla. Despite their membership in Spiralia, gastrotrichs do not apparently undergo spiral cleavage; this trait may have been lost or modified beyond recognition (Dunn, 2008). Nonetheless, several phylogenetic reconstructions have borne out this hypothesis.
While it is clear that gastrotrichs are spiralians, their placement within that clade is more ambiguous. None of the reviewed analyses placed Gastrotricha near the so-called trochozoans, which include annelids and mollusks (Dunn, 2008; Todaro, 2006; Edgecombe, 2011). Their position must therefore be near the remaining spiralian clades: Platyhelminthes and Gnathifera. This grouping of Gnathifera + Platyhelminthes + Gastrotricha is referred to as Platyzoa, though some controversy remains as to whether Platyzoa is a true clade or an artifact of long-branch attraction (Dunn et al., 2008).
Different datasets and methods of analysis have placed Gastrotricha in different positions within Platyzoa. Dunn et al. (2008) found Gastrotricha to be sister to the Platyhelminthes with very weak bootstrap support. They used a broad sample of 71 metazoan taxa and analyzed 150 genes in total. (Not all genes were available for each sampled taxon.) While the study overall used both maximum likelihood and Bayesian strategies for tree-building, after using maximum likelihood they pared down the dataset to include only stable taxa in their Bayesian analysis. Gastrotricha was determined to be unstable. In short, this study found the Gastrotricha to be allied with Platyhelminthes, but inconclusively.
In contrast, Todaro et al. (2006) placed Gastrotricha next to the Gnathifera, a clade of Cycliophora + Micrognathozoa + Rotifera. This study used a smaller dataset, sampling only the genes for small subunit ribosomal RNA. A cladogram constructed using Bayesian analysis gave stronger bootstrap support (77%) to this sister grouping than the support in Dunn et al. (2008) (<70%), but not enough to be definitive. Edgecombe et al. (2011), in a review that included both of these studies, declined to resolve the relationship between platyzoan taxa at all, although they accept Platyzoa as a monophyletic clade. In the end, the position of gastrotrichs in the metazoan phylogeny is uncertain.
This uncertainty is intimately entwined with the general dearth of research on gastrotrichs. While a significant number of gastrotrichs have had limited gene sequencing done, wider genomic data is lacking. Complete sampling both across genes and across taxa is critical to resolving the relationships of unstable phyla like Gastrotricha (Dunn et al., 2008). Increasing the representation of taxa closely related to Gastrotricha in analyses may help in placing the phylum while carrying out studies specifically focused on Platyzoa phylogenies. More refined mathematical models and data analysis techniques should also improve our ability to delineate relationships between currently unstable metazoan phyla, including Gastrotricha (Edgecombe et al., 2011). More extensive morphological studies of gastrotrichs should also allow us to identify possible apomorphies within Platyzoa, of which there are currently very few. (Edgecombe et al., 2011 noted only direct development as a hypothetical apomorphy.) A great deal of work remains before gastrotrichs can claim their proper place in the tree of life.
This work is unquestionably important. Although phyla like Gastrotricha may be obscure, their histories provide vital clues to reconstructing the story of animal evolution and give context to life’s current diversity (Schmidt-Rhaesa, 2002). In particular, their characteristics give supporting evidence to reconstructions of ancestral animal states, allowing us to picture organisms as they were millions of years ago and understand how those states constrained the evolution that produced all animals alive today. Gastrotrichs, if relatives to platyhelminths and rotifers, could provide insight into some of the most destructive human and animal parasites and into the most ubiquitous freshwater animals. Additionally, they may illuminate the nature of Cycliophora, a bizarre phylum of microscopic commensals to lobsters with only a handful of recognized species, discovered less than 20 years ago. The best available evidence suggests that gastrotrichs are related to these phyla, which comprise Platyzoa. It is now up to scientists to muster the will to spend effort on this “lesser known” phylum.
- Dunn, C.W., A. Hejnol, D.Q. Matus, K. Pang, W.E. Browne, S.A. Smith, E. Seaver, G.W. Rouse, M. Obst, G.D. Edgecombe, M.V. Sørensen, S.H.D. Haddock, A. Schmidt-Rhaesa, A. Okusu, R.M. Kristensen, W.C. Wheeler, M.Q. Martindale & G. Giribet. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745-749.
- Edgecombe, G.D., G. Giribet, C.W. Dunn, A. Hejnol, R.M. Kristensen, R.C. Neves, G.W. Rouse, K. Worsaae, M.V. Sørensen. 2011. Higher-level metazoan relationships: recent progress and remaining questions. Organisms, Diversity & Evolution 11, 151-172.
- Schmidt-Rhaesa, A. 2002. Two Dimensions of Biodiversity Research Exemplified by Nematomorpha and Gastrotricha. Integrative & Computational Biology 42, 633-640.
- Smith, D.G. 2001. Gastrotricha. Pennak´s Freshwater Invertebrates of the United States 4th edn (John Wiley & Sons, New York).
- Todaro, M.A., M.J. Telford, A.E. Lockyer & D.T.J. Littlewood. 2006. Interrelationships of the Gastrotricha and their place among the Metazoa inferred from 18S rRNA genes. Zoologica Scripta 35, 251-259.
- Zrzavy, J. 2003. Gastrotricha and metazoan phylogeny. Zoologica Scripta 32, 61-81.