The Invertebrate Tree of Life

Gonzalo Giribet, Gregory D. Edgecombe

• Publisher: Princeton University Press
• Year: 2020
• ISBN:
  9780691197067
• Topic: Sciences biologiques
• Subtopic: Évolution

The most up-to-date book on invertebrates, providing a new framework for understanding their place in the tree of life In The Invertebrate Tree of Life, Gonzalo Giribet and Gregory Edgecombe, leading authorities on invertebrate biology and paleontology, utilize phylogenetics to trace the evolution of animals from their origins in the Proterozoic to today. Phylogenetic relationships between and within the major animal groups are based on the latest molecular analyses, which are increasingly genomic in scale and draw on the soundest methods of tree reconstruction.Giribet and Edgecombe evaluate the evolution of animal organ systems, exploring how current debates about phylogenetic relationships affect the ways in which aspects of invertebrate nervous systems, reproductive biology, and other key features are inferred to have developed. The authors review the systematics, natural history, anatomy, development, and fossil records of all major animal groups, employing seminal historical works and cutting-edge research in evolutionary developmental biology, genomics, and advanced imaging techniques. Overall, they provide a synthetic treatment of all animal phyla and discuss their relationships via an integrative approach to invertebrate systematics, anatomy, paleontology, and genomics.With numerous detailed illustrations and phylogenetic trees, The Invertebrate Tree of Life is a must-have reference for biologists and anyone interested in invertebrates, and will be an ideal text for courses in invertebrate biology.

• A must-have and up-to-date book on invertebrate biology
  
• Ideal as both a textbook and reference
  
• Suitable for courses in invertebrate biology
  
• Richly illustrated with black-and-white and color images and abundant tree diagrams
  
• Written by authorities on invertebrate evolution and phylogeny
  
• Factors in the latest understanding of animal genomics and original fossil material
  

1

BEFORE ANIMALS

Despite anecdotal results from the early days of molecular phylogenetics (e.g., Field et al., 1988), all extant animals (Metazoa) unite as a monophyletic group, sharing a common ancestor that evolved from unicellular organisms in the Precambrian (Sebé-Pedrós et al., 2017). The nature and age of this ancestor are a matter of intense debate, one that may not be resolved anytime soon for many reasons. Nonetheless, progress has been made in terms of the genomic complement of such an ancestor by comparing the genomes of metazoans and their closely related unicellular holozoans (choanoflagellates, ichthyosporeans and filastereans) (fig. 1.1) with those of other outgroups (e.g., King et al., 2008; Sebé-Pedrós et al., 2017; Paps and Holland, 2018; Richter et al., 2018) and reconstructing the common repertoire of genes found across metazoans (see Lewis and Dunn, 2018).

This has shown that the addition of novel groups of genes at the node that leads to Metazoa is considerably larger than the novel genes at any nodes surrounding it. Indeed, 25 groups of metazoan-specific genes have been established as essential for this clade (Paps and Holland, 2018), facilitated by the complete genome sequences of four unicellular holozoans (Sebé-Pedrós et al., 2017): two choanoflagellates (Monosiga brevicollis and Salpingoeca rosetta), a filasterean (Capsaspora owczarzaki), and an ichthyosporean (Creolimax fragrantissima) (King et al., 2008; Fairclough et al., 2013; Suga et al., 2013; de Mendoza et al., 2015). This data set enables reconstructing the gene content of the unicellular ancestor of animals at an unprecedented level of detail—including the so-called multicellularity genes that have roles in cell–cell recognition, signaling, and adhesion. The study of these genomes resulted in a quite surprising result; although there has been gene innovation at the origin of Metazoa (see Paps and Holland, 2018), the unicellular ancestor of animals already had a rich repertoire of genes that are required for cell adhesion, cell signaling, and transcriptional regulation in modern animals (Sebé-Pedrós et al., 2017).

Another recent study, sampling transcriptomes of nineteen additional choanoflagellates, also suggested that a large number of gene families were gained at the stem of Metazoa (Richter et al., 2018). However, whereas Paps and Holland (2018) estimated that the number of gains was much larger than the number of losses, Richter et al. (2018) found that these numbers are very similar, which has been portrayed as evidence for an “accelerated expansion of gene families” versus an “accelerated churn of gene families” along the metazoan stem (Lewis and Dunn, 2018). Perhaps most important, the new study thoroughly sampling choanoflagellate transcriptomes has provided evidence that hundreds of gene families previously thought to be animal-specific, including Notch, Delta, and homologs of the animal Toll-like receptor genes, are also found in choanoflagellates (but not in the two highly derived, previously sequenced genomes) and thus predate the choanoflagellate–metazoan divergence. It is anticipated that the early history of the animal gene repertoire will continue to be refined as the genomes of more closely related holozoans are brought into the picture.

FIGURE 1.1. Top: phylogenetic position of Metazoa among Holozoa and other eukaryotes. Bottom: a timeline of major events leading to the origins of metazoans. Based on Sebé-Pedrós et al. (2017).

The history of the origins of metazoans goes back to Haeckel and Metschnikoff (see a recent historical account in Nielsen, 2012a). Among historical hypotheses, Remane (1963) argued explicitly for a colonial spherical choanoflagellate as an ancestor to Metazoa, instead of the hypothesis of a multinucleated plasmodial cell (e.g., Hadži, 1953), a hypothesis that at least is supported from a sister group perspective between Choanoflagellatea and Metazoa. However, from a traditional morphological perspective, reconstructing the nature of the oldest metazoan requires optimization of characters on phylogenetic trees. Optimizing characters on a well-resolved phylogeny is especially difficult when few characters are shared between the deepest nodes. Supposing that groups like Ctenophora, Porifera or even Placozoa were the first offshoots of animal evolution, meaningful character optimization would be reduced to a handful of molecular markers and subcellular structures, something that would not help us in reconstructing the external morphology of an ancestor.

Likewise, such characters are unlikely to be recognized in the fossil record and thus if the last common ancestor of all animals looked like a comb jelly, a sponge, or a placozoan they would be recognized as stem groups of each of those three lineages, but probably not as the so-called Urmetazoan. Only one scenario, that of sponge paraphyly at the base of the animal tree, would provide the necessary power to say something about such an ancestor, as proposed by Nielsen (2008) in his “choanoblastaea” hypothesis. Sponge paraphyly is, however, disfavored in most recent phylogenetic analyses of sponges and metazoans.

Two facts are important for this book. First is the position of Metazoa in the broader tree of life within a clade of Opisthokonta named Holozoa. Holozoa includes, in addition to animals, choanoflagellates, filastereans and ichthyosporideans. Metazoa is well supported in all molecular phylogenetic analyses as sister group of Choanoflagellatea (e.g., Torruella et al., 2015) [fig. 1.1]. The resemblance of choanoflagellates to sponge choanocytes is striking and has been used a synapomorphy for the clade containing choanoflagellates and metazoans (= Choanozoa), reinforced in those topologies that suggest sponge paraphyly at the base of animals (Nielsen, 2012a). However, few real comparisons have been made between choanoflagellates and choanocytes until recently (Mah et al., 2014), and these authors indicated that although these cells are similar in some aspects, they differ in others, concluding that homology cannot be taken for granted. Similarities in collar-flagellum systems separated by 600 million years of evolution, whether homologous or convergent, suggest that these form important adaptations for optimizing fluid flow at microscale levels (Mah et al., 2014).

Irrespective of whether or not these two cell types are homologous, animal biologists have much to learn from animals’ closest relatives. The first choanoflagellate genome, for the unicellular species Monosiga brevicollis, was thus sequenced to better understand the transition to multicellularity and tissue integration in metazoans. This genome, consisting of approximately 9,200 intron-rich genes, includes genes that encode for cell adhesion and signaling protein domains that were thought to be restricted to metazoans (King et al., 2008), but abundant domain shuffling followed the separation of the choanoflagellate and metazoan lineages. Nonetheless, a series of molecular synapomorphies of metazoans is still supported in the presence of special signaling, adhesion, and transcriptional regulation factors, including Wnt, Frizzled, Hedgehog, EGFR, classical cadherin, HOX, ETS, and POU, or the exclusive metazoan extracellular matrix components such as collagen type IV, nidogen, and perlecan. A list of core animal-specific gene families is given in Richter et al. (2018).

Second is the age of the oldest metazoan fossils, a much more controversial matter (see Sperling and Stockey, 2018, for a recent review). We begin this section by discussing some key paleontological facts and hypotheses in relation to the origin of metazoans.

WHAT IS A METAZOAN?

Defining Metazoa as a term is not trivial, and we now mostly recognize monophyletic groups as they are defined in phylogenies. Metazoa therefore includes any organism that shares a common ancestor with Ctenophora, Porifera, and Bilateria but excludes Choanoflagellatea. We do not consider here therefore the plethora of “protozoan” groups that used to be included in some textbooks as “unicellular animals,” for these are not necessarily the closest sister groups of animals. Metazoans are organisms of multicellular organization, as opposed to unicellular or colonial ones, which means that there are special cell–cell junction molecules (Leys and Riesgo, 2012). That said, multicellularity is not exclusive to metazoans, as it occurs in multiple lineages of eukaryotes, even within Opisthokonta (Ruiz-Trillo et al., 2007). This has allowed division of labor, and even the simplest extant metazoans have multiple cell types.

All metazoans are also ingestive heterotrophic, but that is not equivalent to having a mouth, as pinocytosis and phagocytosis are the sole feeding mechanism of sponges and extracellular digestion with endocytosis by the lower epithelium occurs in placozoans. Virtually all other free-living metazoans ingest food through a mouth, with some exceptions of parasitic or symbiotic species. Nevertheless, the ability of metazoans to phagocytize food is unique among the multicellular eukaryotes (Mills and Canfield, 2016). A prevalent hypothesis is that the first metazoans—the common ancestor of all living metazoans—likely subsisted on picoplankton (planktonic microbes 0.2–2 μm in diameter) and dissolved organic matter, as sponges do nowadays and that therefore, through their feeding, helped bridge the strictly microbial food webs of the Proterozoic Eon (2.5–0.541 billion years ago) to the more macroscopic, metazoan-sustaining food webs of the Phanerozoic Eon (the past 541 mllion years) (Mills and Canfield, 2016). This hypothesis, however, relies upon a similarity between the last common ancestor of modern metazoans and modern sponges. Alternative phylogenetic hypotheses placing ctenophores more basally than sponges have been informally criticized for requiring carnivory to have evolved at the base of the animal tree, but this is not necessarily the case, as extant ctenophores seem to have diversified relatively recently, and there could have been other ecologies earlier in the stem ctenophore lineages. Furthermore, it is difficult to predict the feeding mode of possible extinct stem metazoans, but it is not unlikely that they would have fed on phytoplankton, as many animal larvae do nowadays.

Because multicellular animals must begin as unicellular, metazoan development shares some basic principles in sexual animals. While most nonsexual species tend to have sexual sister species, a few lineages of long-term asexual (mostly parthenogenetic) animals are supposed to exist, for example, bdelloid rotifers (Mark Welch and Meselson, 2000). This phenomenon has, however, recently been disputed, suggesting that bdelloids may have some sort of infrequent or atypical sex, in which segregation occurs without requiring homologous chromosome pairs (Signorovitch et al., 2015). Therefore, the presence of eggs and sperm cells could be considered the typical metazoan condition. After fertilization, metazoan zygotes develop from one of the four cells resulting from meiosis, whereas the other three cells become polar bodies and often degenerate. Embryogenesis in animals is, however, extremely diverse, and polar bodies can carry information or have specific functions. For example, they are key in fertilization of eggs in parthenogenetic animals, or have a role as extra-embryonic tissue in some parasitic wasps (Schmerler and Wessel, 2011).

Some authors have also attempted to identify metazoan-specific markers, including special glycoproteins such as collagens (a large family of proteins found in the extracellular matrix of metazoans), protein kinase C for cell signaling, or even specific neurotransmitters, but many of these molecules are now known from the genome of Monosiga brevicollis, suggesting a premetazoan history of protein domains required for multicellularity (King et al., 2008), and even neurotransmission may have a common origin with the primordial secretion machinery of choanoflagellates (Burkhardt et al., 2011; Hoffmeyer and Burkhardt, 2016). Some recent research may indicate that while fibrillary collagen motifs evolved in the common ancestor of choanoflagellates and metazoans, fibrillary collagen with covalent cross-links between individual fibrils are metazoan synapomorphies (Rodriguez-Pascual and Slatter, 2016). From these, type IV collagen or a type IV–like form (spongin short chain collagen) is present in the basement membrane of all metazoans (Leys and Riesgo, 2012). TGF-ß is also found in all animals but nowhere outside animals, although there are some differences in the complement of genes between sponges and ctenophores with the rest of animals (Pang et al., 2011).

In addition to protein-coding genes, animal cis-regulatory complexity (i.e., distinct enhancers and transcription factor binding sites for different genes that regulate their spatial and temporal expression), once thought to be the trademark of complex animals, is now known to be present in sponges (Gaiti et al., 2017; Hinman and Cary, 2017), but this has not been studied in ctenophores or placozoans.

Germ cells play a unique role in gamete production and thus in heredity and evolution. They can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis) (Extavour and Akam, 2003). At the molecular level, metazoans seem to share a germline multipotency program (GMP) with 18 GMP genes present in representatives of sponges, ctenophores, cnidarians, and bilaterians (...