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Updated: 2 Jan 2006

Animalia

Abstract

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Keywords: yyy

Introduction

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Phylogeny

Plants, Fungi and Animals

Multicellularity reached its culmination in the three great kingdoms of Plants (metaphyta), Fungi, and Animals (metazoans).

Fig 5: A scaled cladogram [after Heckman et al. 2001, fig. 3] depicting lineage divergences of the three major megascopic kingdoms.

...

The rRNA study upon which fig. 1 is based did not resolve the branching of the three familiar, ‘everyday’ kingdoms of plants, fungi and animals. Intuitively, plants and fungi seem to be most similar: they lack the nervous system and muscular activity which characterises animals. In fact, though, the biochemistry of fungi, and the synthesis of chitin in particular, is an apomorphy they share with animals. Thus, plants are likely to have diverged first, leaving fungi and animals as sister groups, although these relationships can not be said to have been resolved beyond all doubt. It appears that the divergences which led to the three ‘everyday’ kingdoms were closely placed in time.

(See Baldauf & Palmer 1993. However, also see Hedges 2002 for discussion of many inconclusive specifics.)

fig. of UToL cladogram

Origins

A molecular analysis of multiple proteins by Heckman et al. 2001 (fig. 5) places the age of major divergences within the fungi at 1,458 to 966 Ma, the appearance of terrestrial fungi at 1,300 ± 100 Ma, divergence of the green algae at 1,061 ± 109 Ma, and the divergence of bryophytes (implying plants on land) at 703 ± 45 Ma (p. 1131).

The protostome-deuterostome (P-D) divergence is placed at ~1,000 Ma by Heckman et al. 2001 and as long ago as 1,200 Ma by Wray et al. 1996. These and other molecular clock studies are further discussed below (see Section 6.5).

"An increasingly well resolved Proterozoic fossil record documents the late Mesoproterozoic to early Neoproterozoic [~1,000 Ma] presence of most of the major clades (kingdoms) of eukaryotes, including the rhodophytes, stramenopiles, alveolates and green plants. A coincident rise in acritarch diversity, combined with molecular phylogenetic evidence for rapid cladogenesis, points to a major radiation of eukaryote groups at this time, sometimes referred to as the ‘big bang’ of eukaryotic evolution" (Butterfield 1999; Conway Morris 2000 also dates this event at ~1,000 Ma; for further reading refer to Sogin 1994).

[Also see Wang et al. 1999]

Trace Fossils

Pre-Vendian trace fossils have been occasionally reported, though most are quickly rejected as pseudofossils. One claim, which appears to be clinging to life for the moment, is for 1,200 Ma traces from the Stirling Range Formation of southwestern Australia (Rasmussen et al. 2002). An earlier claim, for 1,000 Ma branched traces from the Chorhat Sandstone of central India (Seilacher et al. 1998) now seems to be very unlikely: the age constraints on the Chorhat are poor – the rocks could be as young as 540 Ma – and branching of the traces implies a behavioural sophistication not found elsewhere until around 560 Ma (Brasier 1998; also see Rai & Gautam 1999 for an alternative critique).

If either of these traces is real, it implies the existence of bilaterian metazoans circa 1 Ga. While this conclusion is consistent with some molecular clock studies (see Section 6.5), on the balance of present evidence, these claims must be regarded with great doubt.

Other Lines of Evidence

A dramatic decline in the diversity of stromatolites occurring at the end of the Riphean (~ 805 Ma, reference?) has been attributed to the rise of grazing animals (Runnegar 1982, p. 400, and references therein). However, this view was promoted before there existed a widespread appreciation of the snowball events. Given the uncertainty surrounding absolute dates, the onset of the Sturtian glaciations (~700 Ma) may afford sufficient explanation on its own.

However, before moving on, some mention must be made of the systematics of stem group metazoans, many of which have been recognised as discrete phyla – most famously by the Cambridge Burgess Shale revisionists, Harry Whittington, Simon Conway Morris, and Derek Briggs. This view was publicly championed by the late Stephen Gould (1989) and will probably always be associated with his name, although McMenamin & McMenamin 1990 makes vastly more ambitious claims [sidebar ®].

In The Emergence of Animals, Mark and Dianna McMenamin "claimed up to a hundred [most modern textbooks list about thirty] animal phyla ‘exploding’ into life in the Cambrian; most of them are also claimed to have died out, leaving no progeny. ... This view out-Goulded Gould ten-fold. The extraordinary thing to an objective reader is that there is no attempt to justify why these hundred or so ‘Cambrian phyla’ should be recognised. ... Not a word. ... One is driven to the conclusion that these particular writers regard it as only necessary to appear on the Cambrian stage dressed in any sort of odd costume to be called a phylum" (Fortey 2000, pp. 134-135).

While some of the famous Burgess Shale problematica remain incertae sedis, the majority are simply arthropods. As noted by Richard Fortey (2000, p. 127) in commenting upon some earlier cladistic work (Briggs & Fortey 1989), "What surprised us was how easily we could produce a tree relating nearly all of the Burgess Shale arthropods. Graeme Budd adds, "No one would dispute that these fossils are problematic, in the sense that they are difficult to understand. However, that methodological difficulty should not be confused with the possibility that these fossils have only remote affinities with all living groups" (Budd 1997, p.125). Finally, in a subsequent change of heart, Simon Conway Morris has now come to hold forth similar views himself (e.g. Conway Morris 1998), also noting "it is increasingly clear that many of the supposedly ‘bizarre’ animals that have been found at the famous Burgess Shale fossil site in Canada and equivalents elsewhere, especially Chengjiang in China, are actually representatives of phyla in the making. Such a view of the early animal record is, of course, revolutionizing our understanding of how body plans develop as functional entities in a historical context" (book review of Parker 2003, American Scientist Online, 91 (4), July-August 2003).

Eumetazoa

Triploblasta

Diploblastica – the "non-bilaterians" (Porifera, Cnidaria and Ctenophora) - exhibiting radialian cleavage. It is not suggested, however, that these comprise a monophyletic clade.

The Protostome-Deuterostome Dichotomy

The most fundamental division within the bilateral animals is the protostome-deuterostome branch. "Despite wildly different phylogenetic scenarios espoused by different workers, the distinction between these branches has been relatively well-supported. The characters used to establish or support this classic branching are chiefly developmental: Protostomes have spiral cleavage and usually mosaic development, form the mouth at (or near) the site of the blastopore, form mesoderm from a mesentoblast that is usually 4d, and are schizocelic; deutoerstomes have radial cleavage and usually regulative development, form the mouth away from the blastopore, form mesoderm from endodermal cells along the archenteron, and are enterocelic. These basic criteria can be found in almost every invertebrate textbook" (Valentine 1997, p. 8001).

No universal agreement has yet been reached about the exact placement of every animal phylum within one or other group; however:

The protostomes include at least the annelids, arthropods, molluscs and platyhelminthes.
The deuterostomes include at least the echinoderms and chordates, the latter group of course including the back-boned animals.

Newly available evidence from gene sequencing (typically small subunit rRNA phylogenies) have generally supported the broad protostome-deuterostome concept despite challenging the particular assignment of some difficult taxa (e.g. the pogonophorans, classically regarded as deuterostomes) to one clade or the other.

Paraphrase: Although it has been known from the first that some of the taxa assigned to each clade do not display all characteristics in a pure form, it is usually assumed that any anomalies are secondary modifications. There is no general explanation for the association of cleavage pattern with the other characteristics ... point of Valentine's article ... "a shift in cleavage planes in early development."

The fossil record contains trace fossils, presumably of bilaterian animals, at an age of around 565 million years (Ma) (e.g. Bowring et al. 1993). However, no body fossils exist to shed light on a common protostome-deuterostome ancestor. Valentine (1997, p. 8004) speculates that such a creature was a deuterostome (in the sense that the mouth formed apically) with holoblastic radial cleavage, possessing "in all likelihood, vascular fluid, either in a hemocoel or vessels or both, suggesting that the adult was not flat and was not minute, consistent with [the trace fossils]." A modern organism of this structural grade would be considered a pseudocoelomate.

Subdivision of the Protostomia

rRNA data supports the idea that the protostomes are further subdivided into two major clades: the Lophotrochozoa which is a concept that has been around for yonks -- verify -- and the Ecdysozoa, moulting animals, first formally recognised by Aguinaldo et al. in 1997.

Valentine (1997) utilised rRNA and cleavage pattern data to produce a combined phylogeny (fig. 1) identifying five major alliances.

Two of them, the Diploblastica ("non-bilaterians") and Deuterstomia, lie outside the Protostomia. These groups exhibit radialian cleavage.

The three protostome clades are:

Ecdysozoa, including the arthropods and nematodes, with radial cleavage at the deepest branch and idiosyncratic cleavage in the more derived taxa.
Lophophorata, comprising the 'bryozoa' (Ectoprocta), Brachiopoda and Phoronida, with radialian cleavage.
Eutrochozoa, including the Entoprocta, Annelida, Mollusca and Platyhelminthes, which have spiral cleavage, but are interpreted by Valentine to have radialian members at the deepest branches.

Two phyla, the Rotifera and Gastrotricha, are left unassigned between the Eutrochozoa and the Lophophorata; although clustered with the Eutrochozoa in fig. 1, an "alternate possibility, that the rotifers and gastrotrichs branch more deeply than either lophophorates or eutrochozoans, is by no means ruled out. ..."

"Radialians thus lie at the base of each of the major metazoan bilaterian branches – deuterostomes, ecdysozoans, lophophorates, and eutrochozoans. The phyla hypothesized to represent the deepest branches within the ecdysozoans (priapulids) and eutrochozoans (rotifers) are pseudocoelomates, and in general acoelomates and pseudocoelomates occupy the lower branches of those alliances, in accord with available SSU rRNA data" (Valentine 1997, p. 8002).

Although Valentine claims that the Lophophorata group "are united on strong morphologic grounds as well as on the common cleavage pattern" (p. 8001), Neilsen 2001 presents a very different view, considering some members of this group, the Brachiopoda and Phoronida, to lie within the Deuterostomia (see fig. 2). Another and completely different placement for the brachiopods has been further proposed by Conway Morris 1998, mainly on fossil evidence (see below).

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Fig. 1: Valentine's (1997) phylogeny based on major groupings suggested by small subunit (SSU) rRNA data, modified to produce a parsimonious distribution of cleavage types (after Valentine 1997, fig. 1).

However, the earlier view, still vigourously defended in many quarters, ###

Nielsen (2001, e.g. pp. 82 and 119) eschews the Ecdysozoa in favour of a phylogeny derived primarily from morphological features, separating ecdysozoans such as arthropods and nematodes by very fundamental branchings in the protostome clade.

Cladogram of
Metazoan phyla (67452 bytes)

Fig. 2: Nielsen's (2001) phylogeny derived primarily from morphological features (after Nielsen 2001, table 11.1 and fig. 56.3). Note that this view is at variance with lophotrochozoa/ecdysozoa theories.

Fig. 3: A cladogram hypothesising an intermediate role for the fossil group, halkieriids, in the phylogenetic relationship between molluscs, annelids, and brachiopods (after Conway Morris 1998). Note that this view is at variance with the more usual placement of Brachiopoda within the Deuterostomes (e.g. as shown in fig. 1).

1. Metazoa – brachiopods grouped w. bryozoa & phoronida; not mollusca (Valentine 1997, fig. 1)

2. Metazoa ??? – Support for molecular phylogenies provided by cleavage patterns (Valentine 1997, p. 8001)

3. Metazoa – "Deuterostomy is presumably ancestral and is correlated with radial cleavage for this reason, rather than mechanistically" (Valentine 1997, p. 8001).

The Deuterostomes

References

Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, & J. A. Lake, 1997: Evidence for a Clade of Nematodes, Arthropods and Other Moulting Animals. Nature 387: 489-493.

Baldauf, Sandra L.; Palmer, Jeffrey D. 1993: Animals and fungi are each other's closest relatives: Congruent evidence from multiple proteins. Proceedings of the National Academy of Sciences 90: 11558-11562.

Bowring, S.A.; Grotzinger, J.P.; Isachsen, C.E.; Knoll, A.H.; Pelechaty, S.M.; Kolosov, P. 1993: Science, 261: 1293-1298.

Hedges, S. Blair 2002: The Origin and Evolution of Model Organisms . Nature Reviews, v. 3: 838-849.

Nielsen, Claus 2001: Animal Evolution. Second ed. Oxford University Press.

Valentine, James W. 1997: Cleavage Patterns and the Topology of the Metazoan Tree of Life. Proc. Natl. Acad. Sci. USA 94: 8001-8005.