Arthropods and the Origin of Insects

Multicellular life arose in the Precambrian Period. While many animal phyla appear to have originated near the end of the Precambrian (e.g., putative annelids), the first diverse assemblages of animals is not known until the Cambrian, the so-called Cambrian Explosion (Conway Morris, 1979, 1989, 1993, 1998, 2000, 2003). We recognize these lineages as phyla because of the dramatic and fundamental differences in body organization (i.e., each phylum represents a basic groundplan or bauplan for animal design). Among the diversity of ground-plans for building an animal, the phylum Arthropoda, which has achieved a level of evolutionary success unrivaled in evolutionary history, is clearly more dominant on Earth relative to all others. The arthropodan groundplan is the most commonly encountered form of life, having radiated into more species and into more habitats than any other lineage. It is also an ancient phylum, being well represented in the Cambrian faunas by an already impressive diversity, the most famous of which are the familiar trilobites.

Traditionally the arthropods have been considered to belong to a larger grouping of phyla called the Articulata, or the segmented animals (e.g., Cuvier, 1817; Haeckel, 1866; Hatschek, 1878; Snodgrass, 1938; Lauterbach, 1972; Rouse and Fauchauld, 1997; Wagele et al., 1999; Nielsen, 2001; Wagele and Misof, 2001; Scholtz, 2002), and, aside from Arthropoda, to consist of the Annelida, Tardigrada, and Ony-chophora. The latter two phyla comprise, along with Arthropoda, the Panarthropoda (= Haemopoda of Cavalier-Smith,

1998; = Lobopodia of Snodgrass, 1938, although this name is often restricted to Onychophora today) (Figure 3.1). The annelid theory for the ancestry of the panarthropods has been widely recognized (e.g., Brusca and Brusca, 1990) but is increasingly perceived as incorrect. Most recent analyses of morphological and molecular data consider the Annelida distantly related to Panarthropoda (e.g., Aguinaldo et al., 1997; Giribet and Ribera, 1998; Zrzavy et al., 1998a, 2001; Zrzavy, 2001, 2003). Annelid worms are alternatively believed to be related to the Mollusca and Sipuncula, while panarthropods are allied to a series of phyla that are characterized by the absence of locomotory cilia and the presence of a trilayered cuticle (consisting of multilayered epicuticle, exocuticle, and chitinous endocuticle), which molts as they grow via ecydsteroid-induced cycles. This larger clade of moulting animals, referred to as Ecdysozoa (Aguinaldo et al., 1997), consists of the Panarthropoda sister to the Nematoda, Nematomorpha, Kinorhyncha, Priapula, and Loricifera (e.g., Zrzavy, 2003) (Table 3.1). The Ecdysozoa itself is apparently sister to the enigmatic and little understood phylum Gas-trotricha (e.g., Zrzavy, 2003), a small group of microscopic worms inhabiting aquatic habitats.

The Pentastomida, a phylum formerly included in the "Articulata," includes enigmatic parasitic worms (about 95 species) that live in the lungs or nasal passageways of various vertebrates (Storch, 1993). Like the panarthropods, pentasto-mids have a nonchitinous cuticle that is periodically molted

3.1. Phylogeny of panarthropod phyla, the Onychophora, Tardigrada, and Arthropoda; and relationships among the four subphyla of arthropods under the schizoramian (A) and mandibulate (B) hypotheses.

3.1. Phylogeny of panarthropod phyla, the Onychophora, Tardigrada, and Arthropoda; and relationships among the four subphyla of arthropods under the schizoramian (A) and mandibulate (B) hypotheses.

Water Bear Classification

TABLE 3.1. Hierarchical Classification of Ecdysozoa

—ECDYSOZOA— Phylum Gastrotricha (gastrotrichs) Introverta Nematoida Phylum Nematoda (roundworms) Phylum Nematomorpha (hairworms) Cephalorhyncha (= Scalidophora) Phylum Priapulida (priapulans) Scalidorhyncha

Phylum Kinorhyncha (mud dragons) Phylum Loricifera (loriciferans) Panarthropoda

Phylum Onychophora (velvet worms) Tritocerebra Phylum Tardigrada (water bears) Phylum Arthropoda

3.2. A modern velvet worm, Peripatus sp. (Peripatidae), from Panama. Onychophora is a small phylum of approximately 100 living species closely related to arthropods. Photo: P. J. DeVries.

during growth, and the principle body cavity is a hemocoel. However, the nervous system is Crustacean-like, the larvae are nearly identical to Crustacean larvae, and sperm structure and embryogenesis are identical to crustaceans (Wingstrand, 1972; Riley et al., 1978; Storch and Jamieson, 1992). Molecular data have also supported a crustacean origin of the pentastomids (Abele et al., 1989). Indeed, it is now hypothesized that pentastomids are highly derived Crustaceans, perhaps near the Maxillopoda (Martin and Davis, 2001), although limited paleontological evidence tends to favor the placement of the group sister to Arthropoda proper (e.g., Walossek and Mûller, 1994, 1998; Walossek et al., 1994; Zrzavy, 2001; Waloszek, 2003).

Despite the controversy surrounding the larger placement of Panarthropoda, extensive evidence indicates that the group is monophyletic.

ONYCHOPHORA: THE VELVET WORMS

The phylum Onychophora, or "velvet worms," consists of approximately 100 species of legged worms that have a pantropical distribution. Living Onychophora are classified into two families, Peripatidae and Peripatopsidae, and are now entirely terrestrial, generally living amongst moist leaf litter in forests (Figure 3.2). Species tend to be predatory, spraying a proteinaceous "glue" from the oral papillae that ensnares their victims, which include snails, worms, and small arthropods. The body is elongate, with a weak cuticle that is finely annulate (pseudosegmentation) and beset with dermal papillae. The true segments have distinct, unjointed lobopods, which on one segment of the head form sensory structures superficially similar to the antennae of arthropods. The phylum has characteristic peribuccal and large oral papillae, and even has a tracheal system like that of the myri-apods and hexapods within Arthropoda.

3.2. A modern velvet worm, Peripatus sp. (Peripatidae), from Panama. Onychophora is a small phylum of approximately 100 living species closely related to arthropods. Photo: P. J. DeVries.

Interest in the Onychophora largely stems from their apparent phylogenetic position among major lineages of Panarthropoda, specifically as basal to the Tardigrada + Arthropoda lineage (e.g., Zrzavy et al., 1998b; Nielsen, 2001). The phylum unites primitive features of typical "worms" (e.g., Nematoda and Nematomorpha) with those of other panarthropods. Numerous fossils from the Cambrian have been allied with the Onychophora (e.g., Dzik and Krumbiegel, 1989; Ramskold and Hou, 1991; Hou and Bergstrom, 1995), including several enigmatic forms from the Middle Cambrian Burgess Shale such as Hallucigenia and Aysheaia (Ramskold and Hou, 1991). These Paleozoic velvet worms are traditionally placed in their own class, Xenusia, and likely are a paraphyletic stem group to modern Onychophora (class Euonychophora), or are stem group lobopo-dians. Xenusians, unlike modern members of the phylum, were entirely marine and had a terminal (vs. ventral) mouth apparently lacking oral papillae. The earlist Euonychophora (i.e., terrestrial and with a ventral mouth), is known from the Upper Carboniferous (Thompson and Jones, 1980); however, the next record of the phylum is not until the mid-Cretaceous Burmese amber (Grimaldi et al., 2002), a vacuum of nearly 200 million years. This gap is probably due to the fact that the soft bodies of onychophorans very rarely preserve in sediments. While the Carboniferous Helenodora is considered basal within Euonychophora (Thompson and Jones, 1980), the Cretaceous amber Cretoperipatus burmiticus (Figure 3.3), is remarkably modern and even belongs to the living family Peripatidae.

3.3. The oldest velvet worm in amber; Cretoperipatus burmiticus (Peripatidae) in 100 myo Cretaceous amber from Myanmar. Onychophorans date from the Cambrian, but this is the only known Mesozoic member of the phylum. AMNH Bu218; preserved length 5 mm; from Grimaldi et al. (2002).

3.4. Earliest fossils of the phylum Tardigrada, from the Cambrian of northern Europe. They are exquisitely preserved as phosphatized replicas. Tardigrades are the closest relatives of arthopods. Scanning electron micrographs; photos: D. Waloszek.

Tardigrades are a small phylum of 840 species of minute animals (generally 200-500 ^m in length) that live in moss, lichens, leaf litter, and freshwater or even marine habitats. Species feed on mycelia, algae, plant cells, rotifers, nema-todes, and even other tardigrades. They are segmented, possess paired, clawed legs, and molt. Based on these traits, other morphological features, and DNA sequences, tardigrades have been placed as the closest, extant relatives of arthropods (Dewell and Dewell, 1996, 1998; Garey et al., 1996; Giribet et al., 1996; Yeo-Moon and Kim, 1996; Nielsen, 2001). General works on the phylum include Greven (1980), Ramazzotti and Maucci (1983), Nelson and Higgins (1990), Dewell et al. (1993), and Kinchin (1994), while Garey et al. (1999) have provided the most recent cladistic analysis of the group. Defining features of the group include the structure of the eyes; the presence of a nerve between the lateral proto-cerebral lobes and the ganglion of the first pair of walking legs; the modification of the anterior claws into stylets; and the absence of a heart and metanephridia. The occurrence of "Malpighian tubules" in some tardigrades is convergent with those seen in arthropods.

The best-known feature of the phylum is the ability of some species to endure extreme conditions in a dormant, or cryptobiotic, state: years, probably even decades, of complete desiccation (Baumann, 1927); temperatures well above boiling point and near absolute zero (Rahm, 1921, 1924, 1925); intensities of X-rays that are more than 100-fold the lethal dose for mammals (May et al., 1964); and pressures more than six times that known in the deepest oceanic trenches (Seki and Toyoshima, 1998). For these reasons, tardi-grades inhabit some of the harshest regions on earth. Six species live in mosses and lichens in eastern Antarctica (Miller et al., 1996). Most species are widely distributed, if not cosmopolitan. The ability of tardigrades to "encyst," to become highly resistant to extreme environmental conditions, has likely been a principal factor in their distribution. Once encysted, tardigrades can easily be carried by wind or in soil carried by other organisms. Eggs are similarly hardy and may also be easily distributed.

The minute size and membranous integument of tardi-grades makes their fossilization by mineralization or compression highly unlikely or undetectable, although tardigrade-like fossils have been described from mid-Cambrian deposits in Siberia (Müller et al., 1995), phosphatized in complete relief and with microscopic detail (Figure 3.4). These specimens differ from living tardigrades by having three pairs of legs rather than four (although homologues of these may be present in one of the fossils figured by Waloszek, 2003), a simplified head morphology, and no posterior head appendages (lateral cirri and clavae: although Waloszek, 2003, considers fine sensorial structures of the fossils to correspond to these traits among

3.4. Earliest fossils of the phylum Tardigrada, from the Cambrian of northern Europe. They are exquisitely preserved as phosphatized replicas. Tardigrades are the closest relatives of arthopods. Scanning electron micrographs; photos: D. Waloszek.

living tardigrades). The Cambrian fossils probably represent a stem group to the living Tardigrada (Walossek and Müller, 1998).

Besides the Cambrian phosphatized tardigrades, the only other fossils are several rare specimens in Cretaceous amber. The oldest of these is Milnesium swolenskyi in New Jersey amber (Figure 3.5); detailed preservation indicates that the structure of its claws and mouthparts are virtually indistinguishable from the living cosmopolitan species M. tardigradum (Bertolani and Grimaldi, 2000). The other amber fossil tardigrades are two specimens in amber from western Canada (Cooper, 1964), 15-20 million years younger than M. swolenskyi. The best preserved Canadian amber specimen was described in its own genus and family, Beorn

Milnesium Swolenskyi

3.5. Milnesium swolenskyi (Milnesiidae), a tardigrade in 90 myo Cretaceous amber from New Jersey. Tardigrades are remarkably durable animals that can persist in dormancy for such extended periods of time (called cryptobiosis) as to challenge concepts on the longevity of individuals. This species is barely distinguishable from a widespread living species. AMNH NJ796; length 0.85 mm.

3.5. Milnesium swolenskyi (Milnesiidae), a tardigrade in 90 myo Cretaceous amber from New Jersey. Tardigrades are remarkably durable animals that can persist in dormancy for such extended periods of time (called cryptobiosis) as to challenge concepts on the longevity of individuals. This species is barely distinguishable from a widespread living species. AMNH NJ796; length 0.85 mm.

leggi (Beornidae), but it bears a resemblance to several genera in the contemporary family Hipsibiidae (R. Bertolani, pers. comm.). The existence of a recently derived tardigrade lineage in the mid-Cretaceous is consistent with origins of the phylum during the "Cambrian explosions" (Gould, 1989), although such morphological stasis, or bradytely, is extraordinary.

Extreme bradytely (Simpson, 1944; Eldredge and Stanley, 1984) is well known, albeit rare, in evolution. Perhaps the most famous examples from the animal fossil record that show little or virtually no morphological change over millions of years are horseshoe "crabs" (Chelicerata: Xiphosura: Limulus), and the coelacanth (Latimeria). The living Atlantic horseshoe crab, Limulus polyphemus, is very similar to a species from the Upper Cretaceous (c. 70 myo), L. coffini (Fisher, 1984). The only living coelacanth, Latimeria chalumnae, is the sole survivor of the Actinistia fishes, which thrived from the Devonian to the Upper Cretaceous, 380-79 myo (Forey, 1984). The tadpole shrimp, Triops cancriformis (Crustacea: Branchiopoda), is another, less well known example. This "oldest known living animal species" (Tasch,

1969; Schram, 1986; Futuyma, 1998) is indistinguishable from 180-myo Jurassic fossils. Bradytely in Triops tadpole shrimp and Milnesium tardigrades may be attributable to their remarkable ability to become dormant. Living T. cancriformis inhabit nonsaline ponds that are often ephemeral. When the water evaporates, desiccated eggs can remain viable in the sediment for nearly a decade, and withstand temperatures of >90°C for short periods of time. Unlike tardigrades, though, adult Triops cannot enter into such dramatic dormancy, nor can they endure the extremes that tardigrades can. Cryptobiosis probably acts as a general adaptation to various environmental conditions, freeing these organisms from developing suites of morphological and behavioral adaptations, and thus slowing the rate of morphological change. Cryptobiotic tardigrades, in fact, are probably the most durable animals.

ARTHROPODA: THE JOINTED ANIMALS

Over three quarters of all species on earth belong to the Arthropoda. Arthropods have become ubiquitous in every habitat on our planet except for the extreme poles. Nearly everyone can intuitively recognize an arthropod, and they have almost universally been recognized as a natural group for centuries. Even Linnaeus (1758), who was a botanist, was able to recognize arthropods as a group. His Kingdom Animalia was divided into several groups of vertebrates (Pisces, Reptilia, Aves, Mammalia) and two classes of animals without backbones: Insecta and Vermes. Linnaeus' "Class Insecta" corresponds to what we now call Phylum Arthropoda.

The arthropods are defined by numerous features (e.g., Lankester, 1904; Snodgrass, 1938; Boudreaux, 1979; Weygoldt, 1986; Brusca and Brusca, 1990). Some of these features are external and internal body segmentation with regional specialization, or tagmosis; a hardened exoskeleton composed of cuticle that is hardened through calcification (mineral deposition) or by sclerotization (protein cross-linking); an exoskeleton composed of articulated plates; body segments that primitively bear paired, articulated appendages (and hence the name Arthropoda, meaning "jointed foot"); frequently paired compound eyes and some median simple eyes; coelom reduced to portions of reproductive tract and excretory system (the main body cavity is an open hemocoel); an open circulatory system with dorsal, ostiate heart; a complete digestive tract; a ventral nerve cord; stepwise growth via molting (which, as we have seen, is not unique to Arthropoda); and muscles striated and arranged in isolated segmental bands and generally in opposing pairs of flexor and extensor muscles. Perhaps one of the most important features of arthropods is their organization into tagma (plural tagmata), or sets of segments specialized into functional units. Tagmosis has allowed arthropods to diversify their overall body design. For example, the pattern of tagmosis is used, in conjunction with other traits, to identify major arthropod groups.

Despite this impressive array of traits, the monophyly of arthropods has been questioned. Tiegs (1947) considered that the arthropods were actually an artificial combination of two unrelated groups: the Myriapoda, Hexapoda, and Onychophora (the "Uniramia") and the Trilobita, Crustacea, and Chelicerata ("TCC" of Cisne, 1974). Tiegs posited that these two groups originated independently from annelid-like ancestors, converging on "arthropod" traits. This hypothesis was later expanded to consider the three TCC lineages as each being independently derived, expanding the polyphyly to four separate origins (Tiegs and Manton, 1958; Manton, 1964, 1966, 1972, 1973, 1979; Anderson, 1973, 1979; Willmer, 1990; Fryer, 1996, 1998). The principal notion behind the Tiegs and Manton hypothesis of independent origins of arthropods is that the various arthropod lineages could not be considered relatives if the putative ancestor of them all possessed anatomical structures that were, hypothetically, nonfunctional (particularly appendicular structures). Alternatively, if character states observed among the arthropod lineages could not be immediately derived from other characters already existing in modern taxa, then these authors did not believe common ancestry could be supported. In their scenario, the use of the limb base (gnathobase) for grinding food in Trilobita, Chelicerata, and Crustacea was fundamentally different from the use of the apex of an appendage in the other lineages (composite in Myriapoda and Hexapoda). All other characters supporting Arthropoda were ignored along with the possibility that mandibular structures had simply diverged in favor of a functional scenario of appendage evolution. Such a concept of "functionalism" is not valid in phylogenetic reconstruction (Kristensen, 1975; Ax, 1984; Weygoldt, 1986). No rigorous study of panarthropod relationships based on molecular or morphological data has been able to convincingly establish arthropod polyphyly. Indeed, every modern study has strengthened the concept of a monophyletic Arthropoda (Field et al., 1988; Turbeville et al., 1991; Wheeler et al., 1993a; Giribet et al., 1996; Giribet and Ribera, 1998; Giribet and Wheeler, 1999; Nielsen, 2001; Regier and Shultz, 2001a).

The complete phylogeny and evolution of Arthropoda is outside the scope of this work and would fill volumes alone. We have provided here only a brief outline of the major lineages of the phylum so as to place the insects in a greater context and for understanding their origin (Table 3.2). The arthropods consist of at least four major lineages (considered subphyla): Marellomorpha, Arachnomorpha, Crus-taceomorpha, and Atelocerata (Hexapoda and Myriapoda). Neontologists and paleontologists differ considerably on their interpretation of the relationships among these groups, mostly concerning the position of the Crustaceomorpha as either sister to Atelocerata (the Mandibulata, supported by most neontologists) or to Arachnomorpha, along with Marellomorpha (the Schizoramia, supported by most paleontologists) (Figure 3.1). Molecular biologists have come in on both sides of the issue and, while providing additional important data, have not generally swayed the conclusion overwhelmingly to one hypothesis or the other. Furthermore, among those authors who favor the Mandibulata hypothesis, there is a schism concerning the monophyly of the Atelocerata. Within Mandibulata the hexapods are either allied to the Myriapoda (the traditional Atelocerata) or to the Crustacea (the Pancrustacea hypothesis). Despite these points of contention, some major groups are generally accepted.

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