Sea Urchins: Biology and Ecology

1

Phylogeny of Sea Urchins

Andrew B. Smitha and Andreas Krohb,    aNatural History Museum, Palaeontology Department, London, UK., bNatural History Museum Vienna, Department of Geology and Palaeontology, Vienna, Austria.

Abstract

The echinoid skeleton provides numerous characters that are useful for phylogenetic reconstruction, allowing broad integration of fossil and extant data. During the last 50 years echinoid research has strongly profited from the advent of cladistics, considerably improving our knowledge of the evolution of sea urchins. The availability of molecular data has further refined this picture, providing independent support for relationships postulated earlier on the basis of morphological data. An analysis of nuclear 18S and 28S sequences shows high congruence with morphology-based trees. Minor areas of mismatch relate to the relationship within cidaroids, the branching order of ‘diademataceans’, the position of Echinoneus and the diversification of Echinacea, thus identifying areas of the tree in need of more extensive taxon and character sampling. The only major mismatch between molecular and morphological data relates to the monophyly of clypeasteroids, which is currently inexplicable. Relationships within camarodont echinoids, in contrast, are less well understood. A combined morphological/molecular analysis involving species from 30 genera provides support for the traditionally identified families within camarodonts, and partially resolves their higher relationships.

Keywords

Echinoidea; Phylogeny; Classification; Diversification; Camarodonta; Fossil record

1 Introduction

With just over 1,000 extant species (Kroh and Mooi, 2011), echinoids represent a numerically relatively small class of marine invertebrates. Nevertheless, they are often a prominent and important component of marine benthic communities, especially at bathyal and abyssal depths and on shallow water hard substrates (e.g., Furman and Heck, 2009; Tuya et al., 2004) and they have left an extensive fossil record (there are at least 10 times as many named fossil taxa as extant ones). For taxonomists, echinoids offer the major advantage that their multi-plated calcite skeleton yields a wealth of phylogenetically useful information, both in the way the test is constructed and in the great variety and complexity of the defensive appendages (spines and pedicellariae) that it carries. Consequently, the taxonomy of extant and fossil taxa was – prior to genome sequencing – based on broadly the same suite of morphological features. This has ensured that fossil and extant taxonomies are to a large extent seamlessly integrated. Here we provide a short review of our current understanding of echinoid phylogenetic relationships and their geological history, drawing from both genetic and morphological information. Because of the focus of this book we pay particular attention to establishing relationships amongst the camarodont regular echinoids.

2 History of Research

The classification of echinoids has come a long way since the onset of zoological nomenclature marked by the publication of the tenth edition of ‘Systema Naturæ’ by Carl Linné (1758), where only 17 species of echinoids (all in the genus Echinus) were described and classified as molluscs within the class Vermes. The early history of echinoid classification was dominated by a group of incredibly productive French and Swiss zoologists and palaeontologists (Jean-Baptist Lamarck, Louis Agassiz, Eduard Desor, Charles des Moulins and Jules Lambert). By 1925, already more than 60 percent of the extant and fossil echinoid species known today had been described (Lambert and Thiéry, 1909–1925; Kier and Lawson, 1978; Kroh, 2010). As the number of known species increased, the classification of echinoids became increasingly subdivided and was revised repeatedly. This early phase has been reviewed in detail by Durham (1966), and the reader is referred to that paper for a discussion of these early classifications. Here we will briefly discuss the history of echinoid classification and changing ideas since then.

In the influential ‘Treatise on Invertebrate Paleontology’, Durham (1966) adopted and slightly modified the classification of Durham and Melville (1957) that was intended to reflect the major natural subdivisions. It recognizes two subclasses: 1) the Perischoechinoidea, including all the Palaeozoic forms as well as post-Palaeozoic cidaroids and 2) the Euechinoidea (all non-cidaroid post-Palaeozoic echinoids). The latter subclass was divided into four superorders, using concepts of Mortensen (1928–51) and earlier authors (e.g., Zittel, 1879):

• Diadematacea (for Aulodonta as used by Mortensen plus the families Echinothuriidae and Pygasteridae)

• Echinacea (for Stirodonta and Camarodonta)

• Gnathostomata (irregular echinoids with a lantern; for Clypeasteroida, Holectypoida [excluding the Pygasteridae], Conoclypidae and Oligopygidae [attributed to the Cassiduloida by Mortensen])

• Atelostomata (irregular echinoids without a lantern; for Mortensen’s Spatangoida and Cassiduloida [excluding Oligopygidae of Duncan and Conoclypidae])

Durham and Melville (1957) had abandoned the subdivision into Regularia and Irregularia, arguing that the migration of the periproct took place relatively late in geological time and possibly occurred several times independently. This classification was attacked by Philip (1965), who advocated the continued usage of the two subclasses. However, because the ‘Treatise’ proved to be an invaluable source containing brief diagnoses for all known echinoid genera, the classification presented within it was widely employed in the scientific community, despite the fact that its groupings were based on a mixture of primitive and derived characters.

Mintz (1968), based on a thorough but unpublished species-level analysis of early irregular echinoids, proposed a revised classification for the superorder Atelostomata. This, however, has several inherent problems as it contains several paraphyletic taxa: Galeropygoida, which were thought to have given rise to cassiduloids by Mintz (1968), and Disasteroida, which he interpreted as ancestral to both holasteroids and spatangoids. Despite the new insights in the evolution of irregular echinoids presented in that work, few later papers followed the classification outlined therein.

The next step in deciphering echinoid ancestry came when Smith (1981) investigated lantern morphology in Lower Jurassic stem group diadedemataceans and compared it to that of extant echinoids, building on the then new data of Konrad Märkel and Margit Jensen. Smith (1981) was able to show that all living echinoids form a monophyletic group and derive from the archaeocidarid/miocidarid lineage. He furthermore showed convincingly that echinothurioids are a primitive sister group to all other echinoids within a monophyletic euechinoids clade. Novel aspects of the classification presented by Smith (1981) were the restriction of Atelostomata to taxa that lacked a lantern in both adult and juvenile stages, and the rejection of the clearly paraphyletic groups Gnathostomata and Aulodonta. Instead he proposed the Neognathostomata for advanced irregular echinoids that had retained the lantern at least at some time during ontogeny.

Jensen (1982) investigated tooth structure, lantern shape and ambulacral plate compounding to elucidate the evolutionary history of Euechinoidea. While the work used cladistic principles in constructing a cladogram for Echinoidea, it was not a numerical cladistic analysis. In her tree, autapomorphies of terminal branches were identified, but no synapomorphies supporting any of the larger groupings. The classification presented by Jensen (1982) does not reflect the pattern of nested clades within irregular echinoids depicted in her tree, but rather lists six superorders of euechinoids, some of which consequently are paraphyletic by definition.

Smith (1984) formalized his classification presented in 1981 and incorporated new data resulting from the study of Jensen (1982). The classification differs from the 1981 version by incorporating a third subclass (Perischoechinoidea) for Palaeozoic non-cidaroid echinoids, and the introduction of the superorder Microstomata for Neognathostomata+Atelostomata.

Since then, revisions of various groups have been carried out, including Smith and Wright (1989), who analyzed the relationships within the Cidaroida, Mooi and David (1996) and Smith (2004), who analyzed holasteroid relationships, and Mooi et al. (2004), who analyzed echinothurioid relationships.

Littlewood and Smith (1995) were the first to investigate echinoid intra-class relationships using molecular data obtained from a large range of sea urchin taxa (nine out of 14 extant orders). This was combined with a numerical cladistic analysis of 45 extant and fossil taxa using 163 morphological characters. There was good agreement between tree topology resulting from morphological and molecular data. Although Littlewood and Smith (1995) did not present a formal revised classification, their results implied that:

1. Euechinoids indeed are a monophyletic sister group of Cidaroida;

2. Echinothurioids are a basal member of this group, sister to all other euechinoids;

3. Irregularia are a monophyletic group containing a neognathostomate and an atelostomate clade;

4. Echinacea are a monophyletic sister group of Irregularia.

Only a few of the resulting groupings are at variance with the classification of Smith (1984):

1. Diadematacea key out as sister group to Irregularia+Echinacea, rather than in the trichotomy suggested by their previous classification;

2. Stomopneustes and Glyptocidaris are resolved as sister taxa to the monophyletic Camarodonta, rather than being members of the stirodont clade (which was not well supported in any of the trees presented).

About a decade later, the study was repeated with a more complete taxon sampling, investigating representatives of 13 of 14 echinoid orders (Smith et al., 2006). A novel approach of this study was the comparison of branching order within the cladogram with the appearance of the clades in the fossil record. The results imply that the fossil record of echinoids is more than 85% complete at family level and at a resolution of 5-million-year time intervals. Likewise, divergence times inferred from molecular clock and relaxed molecular clock models correspond well with those estimated from the fossil record. Again, no revised formal classification was proposed, but tree topology presents only minor differences to the 1984 classification:

1. Pedinoids were found to be a sister taxon rather than a member of Diadematacea;

2. Echinoneus was resolved as a sister taxon to Neognathostomata alone, rather than to Neognathostomata+Atelostomata;

3. Clypeasteroida was found to be paraphyletic by exclusion of Fellaster in maximum likelihood and Bayesian trees.

A cladistic analysis by Villier et al. (2004) investigated the divergence of early spatangoid echinoids, confirming earlier ideas about intra-spatangoid classification, while Stockley et al. (2005) examined relationships amongst the extant spatangoid families using both morphological and molecular data. Barras (2006, 2007) and Saucède et al. (2007) independently studied the divergence of early irregular echinoids, confirming the monophyly of Microstomata, Neognathostomata and Atelostomata. Stem group members of the latter two clades, however, are often difficult to place and their position often depends on taxon and character selection of the particular analysis. Barras (2006) showed that the taxon Galeropygidae is a plesiomorphic grade and Disasteroida is paraphyletic, while Saucède et al. (2007) demonstrated the paraphyly of Pygasteroida, Galeropygidae and Menopygidae.

Kroh and Smith (2010) performed a numerical cladistic analysis of echinoid morphology (excluding pedicellariae) involving representatives of all nominal family-level taxa. A total of 306 characters were scored for 169 taxa. The analysis resulted in a well-resolved phylogenetic hypothesis, which was used as the basis for a formal classification in which a stem group/crown group approach was followed. Unfortunately, echinoid classification is hampered by two main issues:

1. Deep nodes are commonly not supported by unique apomorphies and higher taxa apparently acquired their own characteristic set of features over time. Diagnoses based on the crown group taxa therefore often fail to encompass fossil stem group members adequately.

2. Tree topology of the lineage leading to irregular echinoids defines a series of nested clades rather than a dichotomous tree, potentially necessitating a high number of ranks even when only major steps in echinoid evolution are to be reflected by the classification.

Comparison of the stratigraphical distribution with the branching order inferred from the cladogram shows high congruence, especially for irregular echinoids. Likewise, the phylogenetic hypothesis presented is in good agreement with tree topology obtained from molecular data (Smith et al., 2006).

Novel aspects of the classification of Kroh and Smith (2010) are:

1. Diadematacea are paraphyletic and rejected;

2. All echinoids with keeled teeth or deriving from forms with keeled teeth form a monophyletic group (named Carinacea by Kroh and Smith, 2010);

3. Stirodonta are paraphyletic and rejected;

4. Cassiduloida sensu Kier (1962) is a paraphyletic grade, as indicated by earlier analyses (Suter, 1994a, b), including many stem group members and had to be restricted in usage;

5. The extinct taxa Plesiolampas, Conoclypus and the Oligopygidae form the immediate outgroups to crown group clypeasteroids.

Their classification is as follows:

Coppard et al. (2012) investigated pedicellarial morphology across all extant echinoid clades, scoring 50 morphological characters for 75 genera of sea urchins. Comparison with the tree topology of Kroh and Smith (2010) showed that homoplasy and secondary loss is frequent in pedicellariae, and that these characters in isolation are unsuitable for higher-level echinoid classification. A combined analysis of pedicellarial characters and the other morphological feature used by Kroh and Smith (2010), however, showed high congruence between the two trees. Although they are not identical (differing in four instances), none of these differences necessitates modification of the higher-level classification.

3 Phylogenetic Relationships

The ever larger and more comprehensive morphological character and gene sequence databases that have been assembled for analysis during the last 15 years have resulted in major advances in our understanding of echinoid phylogenetic relationships. Currently ribosomal gene sequence data exist for many of the major extant clades at superfamily level (e.g. Smith et al., 2006) and the most recent phylogenetic analysis based on morphological data (Kroh and Smith, 2010) has full coverage at family level. Because morphological and molecular data provide effectively independent estimates of echinoid phylogenetic relationships, any congruence between the two corroborates and strengthens our confidence in those particular relationships. Conversely, where the two estimates disagree, one or the other analysis is generating misleading relationships and the support provided by each dataset needs to be examined carefully. In some cases differences will arise through stochastic chance, simply because there are not enough data to resolve particular parts of the tree with confidence. Insufficient phylogenetically informative data result in nodes with low bootstrap support; this is a common problem for both morphological and molecular data. In such cases there is no real conflict between the two independent estimates and the solution with the stronger support after combining the data is to be favored. Conflicting phylogenetic relationships can also arise in which the two datasets each argue strongly for different topological relationships. In such cases there is a serious problem with one or the other dataset and no advance can be made until the source of the problem is understood. Phenomena like nuclear mitochondrial pseudogenes (Numts; Bensasson et al., 2001) represent additional pitfalls and possible sources of mismatch between morphological and molecular data. They are known to occur in echinoids (Jacobs et al., 1983) but are rarely recognized in this group. Here we summarize the areas of congruence and conflict between the two current best molecular and morphological estimates of echinoid phylogenetic relationships.

A molecular database was constructed for the 50 genera of echinoids for which gene sequences of the nuclear 18S-like small subunit and 28S-like large subunit rRNA were available. These taxa comprise representatives from 29 families and 13 of the 14 orders of living echinoids, with new and unpublished data supplementing the alignment used in Smith et al. (2006). Regions where alignment proved ambiguous were removed prior to analysis, so that 3,292 characters were finally used. The concatenated sequences were combined for phylogenetic analysis (data matrix available from the authors). The program Modeltest (Posada and Crandall, 1998) was used to produce an appropriate model of genetic evolution, in this case the GTR+G+I model (rates set to gamma, with six substitution types). Maximum likelihood analysis was carried out in the program PAUP∗ (Swofford, 2002) with empirically deduced nucleotide frequencies and assumed proportion of invariant sites as none. For rooting the tree, we included one taxon from each of the other four extant classes of echinoderms. The resultant tree is shown in Fig. 1.1.

Fig. 1.1 Phylogram of higher-level echinoid relationships derived from maximum likelihood analysis of partial gene sequences of the nuclear 18S-like small subunit and 28S-like large subunit rRNA.

For our morphology-based tree we took the maximum parsimony tree of Kroh and Smith (2010, Fig. 2) and removed all families not represented in the molecular analysis. The cladogram was rooted on Archaeocidaris, a late stem group echinoid. The morphological and molecular phylogenies are compared in Fig. 1.2. From this it is clear that there is a great deal of congruence between the two estimates. The following relationships are supported by both molecular and morphological data and can therefore be considered as securely supported (numbers refer to nodes in Fig. 1.2):

• a basal dichotomy separating Cidaroidea and Euechinoidea (1);

• a basal dichotomy amongst euechinoids separating a clade of echinothurioids from the rest;

• a large clade comprising almost all irregular echinoids (2);

• within irregular echinoids, a major dichotomy between the Microstomata (3) and Atelostomata (4);

• the monophyly of both the Clypeasterina (5) and Scutellina (6);

• a paraphyletic assemblage of cassiduloid taxa with Apatopygidae as the most basal clade;

• a sister group pairing of Holasteroida (7) and Spatangoida (8);

• superfamily relationships within the Spatangoida;

• a large clade comprising the Echinacea (9);

• a clade of Camarodonta (10);

• a clade of Temonpleuridae (11).

Fig. 1.2 Comparison of phylogenetic relationships of echinoids based on morphological and molecular data.

The molecular tree is derived from maximum likelihood analysis of partial gene sequences of the nuclear 18S-like small subunit and 28S-like large subunit rRNA. The morphological tree is derived from parsimony analysis and is equivalent to the best-supported tree in Kroh and Smith (2010) after excising taxa not represented in the molecular analysis. Nodes 1–11 are referred to in the text.

The following regions of the cladogram are those where morphological and molecular trees identify different relationships, but where the support for one or both is low. Thus these represent areas of uncertainty:

• Within the Cidaroidea, both morphological and molecular data lack sufficient characters to resolve with confidence the relationships of the four taxa included, although a Phyllacanthus – (Calocidaris+Prionocidaris+Stereocidaris) pairing is the most strongly supported by molecular data. New results based on 28S and COI sequences by Brosseau et al. (2012) suggest that modern cidaroids are split into three main clades: 1) Goniocidaris+Cidaris+Stereocidaris; 2) Stylocidaris+Prionocidaris+Anthocidaris; which together form the sister group of 3) Psychocidaris+Histocidaris. This arrangement of taxa is compatible with the results of Kroh and Smith (2010), with the exception of the placement of Cidaris, which was rooted within the Stylocidaris+Prionocidaris clade rather than with Goniocidaris in the morphological analysis.

• The relationships amongst the three orders of aulodont (Diadematoida, Aspidodiadematoida and Pedinoida) remain unclear. All three arise after the divergence of the Echinothurioida but before the major radiations of the Carinacea (12) but their order of appearance differs in morphological and molecular datasets. In the morphology-based tree diadematoids are basal, aspidodiadematoids are sister group to the Irregularia and pedinoids are the sister group to the Echinacea. In the molecular tree pedinoids, then aspidodiadematoids, then diadematoids branch off and the Carinacea (12) are monophyletic. However, the character support from morphology is very weak, with no convincing synapomorphies and there is no strongly conflicting signal here.

• The echinoid Echinoneus is placed either as the most primitive irregular echinoid (morphology) or as sister group to the Irregularia (2) + Echinacea (9) clade (molecules). While the position of Echinoneus in the morphological tree is strongly supported, there is only very weak support in the molecular data for the alternative position. Indeed, a molecular tree with Echinoneus in the morphology-based position has a likelihood score that is almost as good.

• Groupings within the Echinacea (9) and Camarodonta (10) are mostly supported by low bootstrap values in the morphology-based tree and by short internal branches in the maximum likelihood tree. Here, more extensive sampling and more data are required from both morphology and molecules before relationships in this part of the tree will be confidently resolved.

There is just one place (starred in Fig. 1.2) where both molecular and morphological data provide strong but conflicting signals, and where further careful analysis of the data is needed for resolution.

• The Clypeasteroida have long been identified as a monophyletic group based on the shared presence of large numbers of tube feet on each ambulacral plate. The two constituent clades Clypeasterina and Scutellina both share this feature and it is found in no other echinoid. By contrast, molecular data identify two cassiduloid clades – the Cassiduloida and Echinolampadoida – as more closely related to Scutellina than Clypeasterina. This implies that the multiplication of tube feet occurred independently in the two clypeasteroid clades. However, if correct, the molecular tree also implies a deep history for Clypeasterina extending far into the Cretaceous, something for which there is currently no evidence. The cause of the mismatch therefore remains unknown and this remains the only part of the tree where morphological and molecular data point strongly to very different phylogenetic histories.

In summary, molecular and morphological data provide corroboration for much of the large-scale structure of the tree and it is largely a lack of data that prevents confident resolution of those parts of the tree where the two data disagree. However, the problem of the monophyly of clypeasteroids remains, despite our more extensive sampling of the Clypeasterina compared to Smith et al. (2006).

4 The Fossil Record of Echinoids

The fossil record of the echinoids starts in the early Upper Ordovician (lower Sandbian), ca. 460 million years (myr) ago (Smith and Savill, 2001) (Fig. 1.3). Echinoids thus first appear a little later than crinoids, asteroids and ophiuroids and approximately contemporaneously with the earliest record of holothurians (Reich, 2001). Molecular data strongly support an echinoid-holothurian sister group relationship (Littlewood et al., 1997; Mallatt and Winchell, 2007), and ophiocistioids, with their large plated tube feet and fully developed Aristotle’s Lantern, are thought to represent an extinct intermediate linking these two groups (Reich and Smith, 2009).

Palaeozoic echinoids are always rare and preserved only under special sedimentary depositional settings. This is because their skeleton was not rigid as it is today, but composed of series of imbricate, membrane-embedded plates and so prone to falling apart rapidly upon death. All Palaeozoic echinoids lived on the sea floor, mouth down, and the most primitive had only sparsely developed small spines, primarily surrounding and protecting the tube feet. In these very primitive forms, ambulacral zones were made up of two columns, as they are today, while interambulacral zones were constructed of a variable number of columns, with plates often rather irregularly arranged. Later in their evolution, echinoids experimented with a number of different ways of building their test, increasing both the numbers of ambulacral and interambulacral columns (Smith, 2005). Furthermore, from the Devonian onwards, echinoids started to develop a covering of large spines (Kier, 1968). Fully functional pedicellariae also appear at this time (Smith et al., 2012), suggesting that predation and parasitization were starting to become a significant problem.

By the late Permian, the first echinoids with tests composed of only 10 ambulacral and 10 interambulacral columns of plates had evolved. They were the only clade to survive the end of the Permian and gave rise to all the modern diversity that we see today. Palaeontological and molecular evidence point to a crown group divergence that dates from around 265 myr ago (Smith et al., 2006).

The post-Palaeozoic record of echinoids is, by contrast, much better documented, as the great majority of echinoids from this time onwards have rigid tests. Fig. 1.3 summarizes the major events, drawing its data from Kroh and Smith (2010). In contrast to other echinoderm classes such as crinoids and ophiuroids (Twitchett and Oji, 2005; Chen and McNamara, 2006; Hagdorn, 2011), echinoids show slow recovery following the End-Permian mass extinction. Cidaroids, which first appeared in the late Permian (Smith and Hollingworth, 1990), were joined by pedinoids in the late Triassic and then by a suite of carinacean taxa in the early Jurassic, including the oldest irregular echinoids and the earliest Calycina and Echinacea. During that period, strengthening of the lantern muscle attachment and improvements in tooth construction can be observed, and the earliest trace fossils recording lantern bite marks appear, suggesting that the preferred diets of echinoids changed, possible in response to new food sources becoming available (Smith, 1984). At approximately the same time, pedicellarial morphology underwent a marked diversification, bolstering the animal’s defensive capability. This implies that echinoids themselves had apparently become an attractive food source for other organisms and/or host for parasites (Coppard et al., 2012).

Fig. 1.3 Stratigraphic distribution of echinoid families through the Phanerozoic.

Each line represents one family. The phylogenetic relationships of families are taken from Kroh and Smith (2010).

During the remainder of the Jurassic, the Phymosomatoida, Salenioida, Stomopneustoida and Arbacioida all flourished in shallow water carbonate settings. The origin of the Camarodonta remains cryptic, largely because the lantern structure in many fossil echinoids remains unknown. What is evident, however, is that by around the mid-Cretaceous stem group members of this clade had evolved. The post-Mesozoic record of regular echinoids, especially camarodonts, is surprisingly poor and possibly marks a shift in facies preference to rocky coastlines and similar hard-ground environments where preservation potential is very low. Cenozoic regular echinoids are rarely preserved in the abundance and diversity seen in the Mesozoic.

The fossil record of irregular echinoids, by comparison, is excellent, largely because they lived in or on unconsolidated sediments where their chances of preservation were much higher. They first appeared during the early Jurassic and specialized as deposit feeders in soft-sediment environments. By the Middle Jurassic, neognathostomate irregulars were both abundant and taxonomically diverse in shallow water carbonate platform settings, while stem group Atelostomates thrived and diversified largely in deeper water, fine-grained clastic settings (Barras, 2008). It is from amongst disasteroids that the crown group atelostomates evolved at the start of the Cretaceous, when both the earliest holasteroids and spatangoids appear in the fossil record. Whereas holasteroids remained much more common and diverse in deeper water settings, the spatangoids expanded in range, successfully colonizing shallow water clastic and carbonate environments during the Cretaceous. Shortly after the end Cretaceous extinction, holasteroids largely disappeared from the fossil record, presumably migrating into the very deep water settings they are found in today (Smith, 2004). Although they can be found in shallow water settings in Australia until the early Miocene, the record of holasteroids in shelf settings in the Northern Hemisphere more or less stops after the Paleocene. Spatangoids, on the other hand, continued to flourish and diversify in shallow water settings world wide to become the dominant irregular echinoid group of today.

Neognathostomate clades thrived and diversified in the Mesozoic shallow water carbonate platform settings, giving rise to a number of clades of cassiduloid echinoids. Amongst these were the forerunners of the clypeasteroids, but it was not until the early Eocene that the first clypeasterines and scutellines appeared. While the various cassiduloid clades declined in diversity after the Eocene, scutellines underwent an adaptive radiation from the late Eocene onwards that gave rise to a number of forms of sand dollar that became specialized for life in shallow subtidal sands where they may form sand dollar beds containing up to several hundred individuals per square meter (Nebelsick and Kroh, 2002).

5 Relationships Amongst the Echinacea

Almost all commercially exploited sea urchins are members of the clade Echinacea and form the core subject matter of this book. A more in-depth analysis of their relationships is therefore attempted here. Thirty-four echinacean genera were selected for phylogenetic analysis (Table 1.1), including four outgroup taxa, two arbacioids (Arbacia and Coelopleurus) and two stomopneustoids (Stomopneustes and Glyptocidaris). A total of 70 phylogenetically informative morphological characters were identified, drawn from Kroh and Smith (2010), Jeffery and Emlet (2003), Jeffery et al. (2003) and Coppard et al. (2012) plus nine additional characters relating largely to larval development and soft tissue traits. Molecular sequence data for 18S, 28S and 16S ribosomal DNA and the mitochondrial gene COI were at least partially available for 30 of these taxa (Table 1.1). The morphological and molecular data were concatenated into a single data matrix, which was then analyzed to find the best supported tree under Bayesian probability (Ronquist et al., 2011), having first defined separate molecular and morphological partitions. An initial analysis that included all 34 taxa had great difficulty in converging on a statistically significant result, and placed those taxa that lacked molecular sequence data in unexpected positions, not supported by analysis of morpholgical data alone. We therefore pruned the four taxa (Evechinus, Parasalenia, Parechinus and Trigonocidaris) for which we had only morphological data and reran the combined analysis. After a run of 1,000,000 generations, Bayesian support had stabilized to give the tree shown in Fig. 1.4.

Table 1.1

Sources of molecular and morphological data for camarodont echinoids (and their immediate outgroups) used in their phylogenetic analysis.

Genebank (www.ncbi.nlm.nih.gov/genbank/) accession numbers for the gene sequences used are listed along with the species whose morphology was scored.

∗currently considered a junior subjective synonym of Heliocidaris (see Hart et al. 2011: 183).

∗∗currently considered a junior subjective synonym of Strongylocentrotus (see Pearse & Mooi 2007: 917).

∗∗∗data from Mortensen (1928–1951) unless otherwise stated.

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bFukushi, T. (1960). The external features of the development of the sea urchin, Glyptocidaris crenularis A. Agassiz. Asamushi Rinkai Jikkenjo Hokoku [Bull. Mar. Biol. Station Asamushi, Tôhoku Univ.] 10, 57–63.

cMortensen, T. (1931). Contributions to the study of the development and larval forms of the Echinoderms. Det Kongelige Danske Videnskabernes Selskabs Skrifter, naturvidenskabelig og mathematisk Afdeling, 9. Række 4, 25–26.

dEmlet, R. B. 2009. The bilaterally asymmetrical larval form of Stomopneustes variolaris (Lamarck). Biol. Bull. (Woods Hole, MA, U. S.) 216, 163–174.

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fMoore, A. R. (1959). Some effects of temperature on development in the sea urchin Allocentrotus fragilis. Biol. Bull. (Woods Hole, MA, U. S.) 117, 150–153.

gClark, D., Lamare, M., and Barker, M. (2009). Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar. Biol. (Heidelberg, Ger.) 156, 1125–1137.

hOnoda, K. (1936). Preliminary note on the experiments of hybridization of some echinoids. Annot. Zool. Japon. 15, 325–333.

iMortensen, T. (1921). ‘Studies on the Development and Larval Forms of Echinoderms’ G. E. C. Gad, Copenhagen, 261 pp.

Fig. 1.4 Phylogram of relationships based on a Bayesian analysis of combined morphological and molecular data drawn from 30 genera of Echinacea. For details see text. Numbers at nodes are posterior probabilities for that clade. Clades are numbered as follows: 1, Stomopneustoida; 2, Echinidae; 3, Strongylocentrotidae; 4, Echinometridae; 5, Toxopneustidae; 6, Temnopleuridae.

Relationships identified from our analysis largely confirm expectations: genera fall into the family groupings of Echinidae, Echinometridae, Strongylocentrotidae, Temnopleuridae and Toxopneustidae exactly as proposed in Mortensen (1943). Furthermore, within those families that had been studied in detail, our combined analysis confirmed earlier results. The relationships amongst the five members of the Echinometridae match those found by Kinjo et al. (2008), our results for the Strongylocentrotidae match those found by Biermann et al. (2003) and our results for the Temnopleuridae are identical to those found by Jeffery et al. (2003). However, the relationships amongst these families are less clearly resolved. The Temnopleuridae are placed as sister group to the remaining camarodont families with high levels of confidence. Within the Echinidea, the Toxopneustidae are identified as sister group to an Echinidae, Strongylocentrotidae and Echinometridae trichotomy, with reasonably high support levels. Lastly the Strongylocentrotidae and Echinometridae are unambiguously identified as clades. Interestingly, despite the rather compelling morphological evidence in support, a grouping of Echinometridae, Strongylocentrotidae and Toxopneustidae did not emerge from this combined analysis. Members of these families have a characteristic projection on their epiphyses that acts as a tooth support (Kroh and Smith, 2010) and distinctively frilled lantern protractor muscles (Ziegler et al., 2012). Neither of these features is present in the other camarodont families. Given the mismatch between molecular and morphological data, this is an area of the tree that requires further investigation.

The phylogenetic positions of Parechinidae, Trigonocidaridae and Parasaleniidae remain tentative due to the lack of molecular data. Morphological data place Parechinus as sister group to Paracentrotus and thus within the family Echinidae, so its treatment as a subfamily of Echinidae by Mortensen (1943) is supported. Similarly Trigonocidaris is placed as sister group to the Temnopleuridae, a position also predicted by Mortensen (1943). Of most interest is Parasalenia. According to its morphology, Parasalenia is either sister group to all other camarodonts (Kroh and Smith, 2010) or sister group to camarodonts plus stomopneustoids (this analysis). The latter arrangement is supported primarily by apical disc morphology but is contradicted by lantern morphology (Parasalenia has a more advanced lantern with fused epiphyses typical for camarodonts, whereas in stomopneustoids the epiphyses are not fused). Clearly these taxa need to be the target of future molecular studies to try to resolve their phylogenetic position with more certainty.

From an analytical point of view, our results show that a large amount of missing data, as exhibited by the molecular data employed here, is not detrimental to the analysis and allows for a broader inclusion of taxa with incomplete datasets. This corroborates similar conclusions reached by Wiens (2003) and Wiens and Moen (2008) based on simulations. There is, however, a certain threshold below which meaningful placement of individual taxa is no longer possible. When taxa were included in the analysis for which molecular data were completely lacking, they were rooted in places inconsistent both with the results from analysis of the morphological data partition alone, as well as traditional taxonomic placement. This likely is an artifact pertaining to the highly skewed relation of known to missing characters, with the latter being almost two orders of magnitude higher in these taxa. Similar instances of misplacement of incompletely sampled taxa have also been observed in other studies combining morphological and molecular data (see discussion of the analysis of Gatesy et al., 2004 by Bininda-Emonds, 2004). Additionally, like Pirie et al. (2008), we found that inclusion of taxa with high percentage of missing data caused prohibitively long computation times for Bayesian analyses. On the other hand, support values in Bayesian analysis appear less affected by the missing data than parsimony and maximum likelihood analyses we carried out on the same dataset.

Here a combined analysis of multiple datasets is superior to separate analyses. Analysis of the individual datasets alone, for example, results in misplacement of Lytechinus (16S rRNA) and Microcyphus (COI) as sister taxa to all other camarodonts, possibly hinting the undiscovered presence of Numts (Bensasson et al., 2001) in these taxa. 18S rRNA data alone performed worst, failing to recognize any of the traditional families except for Temnopleuridae. Separate analysis of 28S rRNA data, in contrast, resulted in a tree fully compatible with the one of the combined analysis. COI data in isolation found radically different branching orders within individual camarodont families, and placed some bona fide echinometrids as basal members of the Strongylocentridae clade. In conclusion we suggest that evidence from multiple gene loci in combination with morphological data performs best in reconstructing true relationships, and may be a viable way to circumvent issues of misplacement due to problems within the individual datasets, even when combining the data results in large amounts of missing data for some of the studied taxa.

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Chapter 2

Sea Urchin Life History Strategies

John M. Lawrence,    Department of Integrative Biology, University of South Florida, Tampa, FL, USA.

Abstract

Life history strategies are based on the characteristics of organisms that affect their fitness. Two environmental factors important in determining the life history strategy of organisms, including sea urchins, are stress, conditions that reduce production and disturbance, partial or total destruction of biomass. Disturbance includes predation. Different characteristics of different life history strategies are associated with different combinations of levels of stress and disturbance. The hypothesis that these characteristics are associated with particular habitats was tested by predicting where sea urchins with particular life history characteristics would occur. The habitats considered (the deep sea, Antarctic waters, tropical reef flats, kelp forests and tropical seagrass beds) differ in the levels of stress and disturbance. Species with different life history characteristics were found in the predicted habitats. Recognition of the life history strategies of sea urchins species is basic to understanding their biology and ecology. Knowledge of the strategies of extant sea urchins is useful for paleobiological and paleoecological studies. Strategies have important implications for fisheries management, conservation and evaluation of species for aquaculture. Habitats may be expected to change with ocean warming and acidification. The response of sea urchin species to the predicted changes may vary with life history strategy.

Keywords

sea urchins; life history strategies; deep sea; Antarctic waters; tropical reef flats; kelp forests; seagrass beds

1 Concepts

Southwood (1977) pointed out that the traits or characters of organisms are wide and varied. He said that the function of theories of life history strategies is to provide a classification into which facts can be arranged. Identification of life history strategies is an attempt to do this. It uses the suite of life history traits of a species from fertilization of the egg to death of the individual that maximize the numbers of their descendants in their habitat. Southwood (1988) described the two-strategy model of MacArthur and Wilson (r-K selection) as selection in relation to density-dependent resource availability. Greenslade (1972) recognized a third type of selection, which favored conservation of adaptation to consistently adverse environments.

Grime (1977, 1979) proposed a three-strategy model based on two factors in an organism’s habitat that affect life history characteristics: stress and disturbance. He defined stress as conditions that restrict production. This would include unfavorable climatic conditions and low levels of nutrient resources. Both are adverse conditions as defined by Greenslade (1972) and Southwood (1977). Grime’s definition of stress is consistent with Levitt’s (1972) analogy of biological to physical stress. In biological systems, stress produces a decrease in production. Since production is expressed in units of energy (Brody, 1945), biological stress results in a decrease in deposition of energy in the organism. Lawrence (1990) considered low levels of nutrient resources, including low quality of food, low availability of food and low ability to obtain food, as stresses because they limit production. The ability to obtain food can be affected by the size and morphology of the animal. It also can be affected by conditions that limit its capacity to forage.

Grime (1977) defined disturbance as partial or complete destruction of biomass that results from predation or physical environmental effects. Sousa (2001) interpreted disturbance as damage or mortality of an organism as the consequence of some external agent or force. Although he stated that his use of the term disturbance was consistence with Grime’s (1977) definition, he restricted disturbance to damage, displacement or mortality caused by physical agents or incidentally by biotic agents. The consequences of death from predation and physical agents are the same. In sea urchins, disturbance is usually death. Steneck (Chapter 14) considers defenses of post-Paleozoic sea urchins constrained by the functional limitations of the spines, and thus they are susceptible to predation. He suggested it may not have been until the Cenozoic evolution of advanced benthic predatory fishes that slow moving sea urchins were at widespread risk of predation. In addition to disruption by predation or physical agents, Grime (2001) pointed out climatic factors such as temperature and salinity are stresses if they only decrease production but are disturbances if they are result in death.

Grime (2001) used the method of Southwood (1977) and Greenslade (1983) to classify habitats by ordinating them within a rectangular space representing variation in productivity and duration (Fig. 2.1). A diagonal connecting habitats with high productivity and long duration separates the rectangle into habitats that are tenable and those that are not. With the four permutations of extreme low and high productivity and short and long duration, only three primary strategies are viable (Grime, 1977). This is because conditions of high stress do not provide the capacity for production necessary for recovery from high disturbance. He suggested the three remaining combinations are associated with three distinct types of primary strategies. He called the primary strategy associated with high disturbance (short duration) and low stress (high productivity) the ruderal strategy (R-strategy) (based on the Latin word for rubble, and thus for plants growing in a disturbed habitat). Such a ruderal strategy for sea urchins would be found in habitats where disturbance (from predation, physical factors or extreme climatic conditions) is high but where there are abundant resources. The primary stress tolerant strategy (S-strategy) is associated with high stress (low productivity) and low disturbance (long duration). For sea urchins, regions with low primary productivity would be stressful habitats. The primary competitive strategy (C-strategy) is associated with habitats with low stress (high productivity) and low disturbance (long duration). Grime (1989) made an economic metaphor of the competitive strategy with biological ‘capitalism’. Capitalism requires a stable society and government (low disturbance) and abundant resources or great ability to obtain resources (low stress). Most habitats are not at extreme levels of stress and disturbance where the three extreme primary strategies would be most conspicuous. Secondary strategies would occur at combinations of intermediate productivities and intensities of disturbance (Fig. 2.2).

Fig. 2.1 Tenable and untenable triangles for habitats ranging from low to high productivity and short to long habitat duration.

Tenable habitats occur above the diagonal; untenable habitats occur below the diagonal. R: Ruderal strategy at extreme high habitat productivity and short habitat duration. S: Stress tolerant strategy at extreme low habitat productivity and long habitat duration. C: Competitive strategy at high habitat productivity and long habitat duration. Secondary strategies occur above the diagonal between the extremes. (from Grime, 2001).

Fig. 2.2 Triangular model indicating the strategies resulting from combinations of different levels of stress and disturbance.

C: competitor, S: stress-tolerator, R: ruderal, CS: stress tolerant competitor, CR: ruderal competitor, SR: stress tolerant ruderal, CRS: CRS strategist. (modified from Grime, 1977).

A suite of traits or characteristics would be predicted for these primary strategies for sea urchins in different habitats (Table 2.1). Because many sea urchin species can exist in a variety of habitats, estimates of these traits can be expected to vary under different conditions. Ebert (1982) astutely pointed out that it is difficult to know if a particular population of a species of sea urchin is in the mainstream of evolution and that this is a recurring problem in studies of field populations that use evolutionary arguments to interpret data. Instead of the a posteriori approach of formulating explanations after observing correlations between traits and the habitat, Sibley and Calow (1986) advocated the a priori approach of making hypotheses about traits that would be predicted in species occurring in particular ecological circumstances. It is necessary to have a thorough knowledge of the habitat to do this. Conditions can be controlled in laboratory studies to complement field observations and allow testing a priori predictions of the response of species to experimental conditions. A priori predictions on the length of survival of different species of sea urchins when starved were confirmed (Fig. 2.3).

Table 2.1

Characteristics of habitats and predicted traits of sea urchins with competitive, stress tolerant or ruderal primary strategies.

Fig. 2.3 Time to death from starvation of Lytechinus variegatus, Echinometra lucunter and Eucidaris tribuloides. (Lawrence and Lares, unpub.).

The interaction of stress and production, and its emphasis on energy, is apparent in the energy budget:

where A is absorption, R is respiration, U is excretion, Pr is reproductive production and Ps is somatic production, all measured in energy units. R includes energy used for physiological maintenance and for anabolism. Complete energy budgets have been used to estimate relative allocation to the gonadal and somatic production for only a few species of sea urchins (Fuji, 1967; Miller and Mann, 1973; Propp, 1977; Hawkins and Lewis, 1982) because of logistics.

Inherent in the budgets are physiological tradeoffs, which Stearns (1992) defined as allocation decisions between two or more processes that compete directly with one another for limited resources within a single individual. An increase in allocation to Pr decreases the allocation to Ps. The interaction of these processes is apparent in the Euler-Lotka equation (Calow, 1984)

where r is the Malthusian parameter (intrinsic rate of natural increase), t is time to maturity (a function of somatic production), s is survival (a function of maintenance and protection) and n is fecundity (a function of gonad production). Tradeoffs are apparent in the traits of life history strategies in Table 2.1.

Ebert (1975) was the first to explicitly link rate of growth and survival in sea urchins. He found a positive correlation between the Brody-Bertalanffy growth constant K and the instantaneous natural morality rate M. Ebert (1982) combined allocation of resources, energy and material to morphology, physiology and behavior that increase the probability of living from time t to t + 1 as maintenance. He proposed that differences in survival rate among species are related to differences in the probability of leaving offspring at each reproductive episode. Little variability in the probability of leaving offspring would result in the strategy of allocating more resources to growth and reproduction and less to maintenance, resulting in a short life span. Great variability in the probability of leaving offspring would result in the strategy of allocating more resources to maintenance and less to growth and reproduction, resulting in a long life span. The probability of leaving offspring could be affected by fecundity and survival and successful settlement of the larvae. Chia (1974) concluded the main selective force for evolving non-feeding larvae from feeding larvae in marine invertebrates was the limitation of energy for gamete production. Lawrence and Herrera (2000) proposed lecithotrophic development, brooding and secondary metabolites in eggs of echinoderms were characteristics associated with a decrease in quality of food or ability to obtain it that would lead to the stress tolerant strategy.

Although resources for echinoderms typically have been considered in terms of energy (Lawrence, 1985), protein is an essential resource for production that may equal or exceed the requirement for energy. Lowe and Lawrence (1976) suggested production by sea urchins may be more dependent on protein than energy. Nutritional studies have demonstrated the importance of protein in production by sea urchins and that the protein:energy ratio of food affects production (Marsh et al., Chapter 4; Watts et al., Chapter 10). This indicates the importance of food quality in addition to the amount of energy.

Stearns (1992) pointed out the ratio of reproductive biomass or energy to that of the parent (an index) is a static measure that does not represent the proportion of mass or energy flowing through the organism that is allocated to reproduction. Hirshfield and Tinkle (1975) noted that individuals of two species could allocate the same quantity of mass or energy to reproduction at equivalent body sizes but differ greatly in the absolute amount of mass or energy consumed or in the time during which it was consumed. In this case, the true proportional allocation to reproduction (reproductive effort) would be unequal, while the ratio of reproductive weight or energy to body weight or energy would be the same. The relative allocation to a process such as reproduction (reproductive effort) is the important consideration, not the absolute allocation (reproductive output) (Lawrence, 1985). Thus the gonad index, which has a long history of use with sea urchins (Boolootian, 1966), indicates reproductive output but not reproductive effort.

2 Habitats and life history strategies of sea urchins

2.1 The deep sea

The deep sea is considered to begin at the edge of the continental shelf, usually a depth of 200 m (Thistle, 2003). Sanders (1968) characterized it as a physically stable environment. The potential for disturbance from predation is low because durophagous brachyuran crabs, lobsters, sharks, rays and teleosts are found primarily in shallow water or on the continental shelf (Aronson et al., 2007). Most accounts of the depth distribution of marine groups emphasize the degree of ability to withstand the potential for predation and do not consider the potential for production. The major stress faced by organisms in the deep sea is the low availability of food and its low quality (Gage, 2003; Thistle, 2003). These conditions result in a low capacity for production. Species that tend towards the stress tolerant strategy with slow growth and great longevity would be predicted to occur in the deep sea.

Sea urchins that have a low capacity to feed, a low growth rate, high survival rate and non-feeding development and brooding would be predicted to occur in this habitat. Cidaroids and echinothuriids are predominantly deep-sea groups (Hyman, 1955). Deep-sea sea urchins include a number of orders that Smith and Stockly (2005) characterized as generalist omnivores that had migrated into the deep sea in small numbers over the past 200 million years.

The biology and ecology of deep-sea sea urchins is little known. Gage and Tyler (1985) estimated Echinus affinus from the Rockall Trough at a depth of 2,200 m lives for up to 28 years and becomes mature after about five years. The shallow water Echinus esculentus lives for only up to 12 years and becomes mature after about 1.5 to 2.5 years (Nichols et al., 1985). Echinus affinus has a small egg and a planktotrophic larva, which would not be predicted for a species with a stress tolerant strategy. However, this may be a phylogenetic constraint as all species of the family Echinidae have this characteristic (Emlet, 1995). All five species of echinothuriids and one species of cidarid from the deep sea studied by Tyler and Gage (1984) produced large eggs characteristic of stress tolerant species. A second species of cidarid produced small eggs. Cidaroids have a slow rate of feeding, slow growth, late maturity (Lawrence and Jangoux, Chapter 16) and would be expected to occur in the deep-sea environment.

2.2 Antarctic seas

Antarctic seas provide a habitat in which sea urchins with a stress tolerant strategy would be predicted to occur. The seas around Antarctica are stereotyped as being oligotrophic with seasonal pulses of high primary productivity in surface waters and shallow depths without ice cover and constant low temperatures (Lawrence and McClintock, 1994). Food resources have been characterized as long-term low availability modified by predictable short-term primary production (McClintock, 1994). The potential for production by sea urchins with these conditions would be low. Habitats in Antarctic seas are physically very stable at depths greater than 30 m (Pearse et al., 1991). Disturbance from predation seems low also. Aronson et al. (2007) noted the absence of durophagous brachyuran crabs, lobsters, sharks, rays and teleosts in Antarctic seas. Species of sea urchins that tend towards the stress tolerant strategy would be predicted to occur in this habitat of high stability, low predation and low production.