The First Arthropods
A variety of marine worms (Annelida and Protoannelida) lived in the ocean sediments during the Cambrian period. These creatures were bilaterally symmetrical, soft-bodied, and multisegmented. They had no distinct head capsule and lacked both eyes and antennae. Some species may have had lobe-like lateral appendages similar to the parapodia of polychaete worms that thrive in the muddy sediments of today's ocean floor. But structural differences between the lateral appendages of polychaetes and early arthropods suggest that these two groups diverged from a common annelid ancestor some 500-600 million years ago. All annelids were soft-bodied. They decayed rapidly after death and were not well-preserved in the fossil record.
At one time, the Onychophora or velvet worms were suggested as a possible evolutionary link (intermediate) between the annelids and the arthropods. These mostly-tropical invertebrates, with only 75 extant species, live on the forest floor among moist, decaying leaves and feed on a mixed diet of plant and animal tissues. Like annelid worms, the Onychophorans have segmented bodies containing paired excretory organs (nephridia) and a combination of both male and female sex organs (monoecious). They lack a true exoskeleton, but the body is covered by a soft, chitinous cuticle. In true arthropod fashion, this cuticle is periodically shed (molted) to allow for continued growth. Onychophorans also share numerous other characteristics with the arthropods, including antennae, an open circulatory system, walking legs with claws, paired mandibles, and a system of slender air tubes (tracheae) for respiration.
Today, the prevailing opinion among modern taxonomists is that Onychophora and Arthropoda represent sister groups (see Cladogram 1), but the issue is far from settled. Both Anderson (1973) and Manton (1977) contend that onychophoran leg structure, locomotion, and embryological development is most comparable to that of the myriapods (millipedes, centipedes, et al.) and a recent comparison of nucleotide sequences in ribosomal RNA of velvet worms and other arthropods also supports a close affinity between these groups (Ballard et al. 1992).
Velvet worms may or may not prove to be direct ancestors of the arthropods, but regardless of classification, it seems reasonable to assume that the very first arthropods were distinctly worm-like in structure and appearance. They were also different in at least one important way: they had an exoskeleton. This structure, secreted by epidermal cells, was more rigid than annelid cuticle and necessitated membranous "joints" to provide the flexibility needed for movement. This exoskeleton (and its jointed appendages) is the hallmark of the arthropods.
A classical controversy that still rages among invertebrate zoologists, including the entomologists, relates to the evolutionary pathway (or pathways) of adaptive radiation that arthropods followed as they gradually diverged from primitive ancestors. The traditional, and certainly more conservative approach, assumes that arthropods arose only once from protoannelid ancestors. This monophyletic argument is based on the observation that many features, such as the exoskeleton, open circulatory system, hemocoel, etc., are shared by nearly all taxa within the group and appear to be homologous (i.e. have the same evolutionary origin). A contrary view is taken by other biologists who argue that arthropod-like organisms must have evolved more than once (perhaps as many as four times) in geological history. Support for this polyphyletic approach is found in embryological development and in comparative studies of the mouthparts and other appendages. Proponents of the polyphyletic hypothesis claim that many similarities between taxa have arisen coincidentally, through the process of evolutionary convergence.
The Monophyletic Hypothesis
All arthropods differ from their annelid ancestors in several important ways: they have a chitinous exoskeleton, jointed/segmented appendages, a well-developed head and mouthparts, striated muscles, and an open circulatory system with a dorsal heart. Unlike annelids, the arthropods produce large, yolk-laden eggs that are encased in a proteinaceous shell. Ciliated nephridia, paired segmental excretory organs found in annelids and onychophorans, have been replaced in arthropods by specialized excretory organs located on the head (green glands in crustacea), near the legs (coxal glands in horseshoe crabs), or in the abdomen (Malpighian tubules in terrestrial arthropods). Remarkable similarities in the chemical composition of the exoskeleton and in the ultrastructure of the compound eyes in organisms as diverse as millipedes, shrimp, and horseshoe crabs provide strong evidence that all of these groups (myriapods, crustaceans, and chelicerates) must have evolved from a common ancestor.
The monophyletic classification scheme, proposed by Boudreaux (Cladogram 2), recognizes three evolutionary lineages within the phylum Arthropoda: Trilobita, Chelicerata, and Mandibulata. The trilobites became extinct by the end of the Permian Era and therefore represent an evolutionary "dead end". Chelicerata includes all arthropods with fang-like mouthparts (chelicerae): spiders, ticks, and mites (Arachnida), horseshoe crabs (Xiphosura), and sea spiders (Pycnogonida). Mandibulata includes all arthropods that have chewing mouthparts (mandibles): crustacea, myriapods, and insects. Early in the Paleozoic Era, the mandibulate lineage divided into at least one group that continued a marine lifestyle (the crustacea), and another group that adopted a terrestrial lifestyle. This terrestrial lineage, which encompasses all present-day myriapods and insects, is known as the superclass Atelocerata, a taxon first described by Heymons in 1901.
Boudreaux's classification scheme excludes onychophorans because they lack a true exoskeleton, but other workers disagree. Meglitsch and Schram (1991) regard the Onychophora as closely related to myriapods. In their monophyletic classification scheme (Cladogram 3), Crustacea and Chelicerata are the most primitive groups. Insects, myriapods, and onychophora are grouped together in the superclass Uniramia because of similarities in leg structure and locomotion.
A great deal of controversy surrounds the evolution of arthropod legs and wings. Proponents of monophyletic classification argue that the legs of all arthropods are homologous (have a common evolutionary origin); opponents claim there is too much diversity in leg structure to justify a single ancestor. Jarmila Kukalová-Peck, a Canadian entomologist, has proposed that "primitive" arthropods may have had as many as eleven segments in each walking leg. She cites evidence from an extinct fossil insect to support her claim that the eight-segmented legs of spiders, the seven- to nine-segmented legs of crustacea, and the five-segmented legs of insects all exhibit some degree of reduction from the "primitive" groundplan.
The Polyphyletic Hypothesis
If we embrace the idea of polyphyletic origins, then arthropods are represented by as many as four major phyla -- each of which is presumed to have evolved separately from primitive annelid ancestors:
- Trilobita -- 4,000+ species -- including all trilobites (extinct marine organisms that were abundant during the Paleozoic era.)
- Chelicerata -- 70,000 species -- including spiders, scorpions, mites, ticks, horseshoe crabs, and sea spiders.
- Crustacea -- 30,000 species -- including shrimp, crabs, lobsters, woodlice, barnacles, amphipods, branchiopods, and copepods.
- Uniramia -- 1.2 million species -- including onychophora, millipedes, centipedes, pauropods, symphylans, and insects.
Evidence to support the polyphyletic hypothesis can be found in the comparative anatomy of appendages and in the embryonic development of the head and mouthparts. Sydney Manton, one of the founders of the polyphyletic hypothesis, suggested that there is a fundamental difference between the appendages of crustacea and those of other arthropods such as insects and myriapods (millipedes and centipedes). Manton argued that crustacean appendages are biramous; that is, two apical units (rami) are attached to a single basal unit. Appendages of other arthropods are uniramous: a single apical segment is attached to a single basal segment. Manton believed that crustaceans evolved from annelid worms similar to marine polychaetes of today, and that all other arthropods evolved from annelid worms that were more similar to the onychophora. This hypothesis is also supported by D. T. Anderson whose studies of arthropod eggs has revealed that initial cell division in crustacean embryos is holoblastic (spiral cleavage), whereas the eggs of all other arthropods are meroblastic (superficial cleavage). The eggs of all known annelids are holoblastic.
Embryological development of the head and mouthparts has also been offered as evidence to support the polyphyletic hypothesis. In myriapods and insects, the head is a separate functional region. But in the crustacea and the chelicerata, the head and thorax develop together as a single body region, the cephalothorax. Furthermore, within the myriapods and insects there is evidence that additional segments are added to form mouthparts, suggesting that the mouthparts of chelicerates, crustaceans, and other arthropods are not homologous.
Regardless of whether we adopt a monophyletic or a polyphyletic classification scheme, it is apparent that the insects have more in common with the myriapods than with any other taxon of the Arthropoda. Insects and myriapods are adapted to a terrestrial lifestyle, exhibit similar embryological development, and share many similarities in the morphology of the head and mouthparts.
The myriapods include both Chilopoda (centipedes) and Diplopoda (millipedes) as well as two other classes that are not as well-known: Symphyla and Pauropoda. All of these organisms live in moist environments near the soil surface (e.g., under stones, amid leaf mold, in rotting wood, etc.). Centipedes are primarily predators, the others are scavengers and herbivores.
All myriapods exhibit ametabolous development (there is no significant change in body form as they mature). Eggs hatch into immatures (called young) that are similar to adults in most respects except size and sexual maturity. Like all other arthropods, they grow by molting, but they may also increase in length by adding an additional body segment at each molt. This type of growth (called anamorphosis) is common in myriapods, but it occurs only rarely in more "advanced" arthropods and is usually regarded as a "primitive" characteristic (pleisiomorphic condition).
Myriapods have only two functional body regions: a head and a trunk. The head is specialized for sensing the environment (eyes and antennae) and ingesting food. The trunk is adapted for locomotion and also contains most of the internal organs. Pauropods and symphylans are generally small (under 5 mm in length) with little or no body pigmentation -- they are frequently creamy white in color. Symphylans have beaded antennae and 10 to 12 pairs of legs. Pauropods have branched antennae, nine pairs of legs, and plates of exoskeleton on the dorsal surface that usually span more than one body segment. Millipedes and centipedes are usually larger (more than 5 mm in length) and dark brown to black (although some species may be quite colorful). Centipedes have at least 15 pairs of legs -- the first pair, immediately behind the head, contain poison glands and are modified as fangs for killing prey. Millipedes have at least 30 pairs of legs, two pair per body segment. They are not as fast-moving as centipedes and often curl into a ball or release a defensive spray as protection from predators.
Most biologists and paleontologists feel that there is sufficient morphological, embryological, and fossil evidence to justify a claim that the basic structural plan of the insect head evolved very early in the myriapod lineage. As the head assumed a more prominent role in the organism's survival, it increased in size and usefulness by assimilating adjacent trunk or body segments that previously had been adapted for locomotion. In this process of cephalization, the leg appendages evolved into mouthparts that became adapted for catching, processing, or manipulating food items. These mouthparts are said to be segmentally homologous with walking legs. Indeed, if this is the case, we might expect to find "primitive" organisms that have only mandibles (monognathous), "less primitive" organisms having both mandibles and maxillae (dignathous), and "advanced" organisms with mandibles, first maxillae, and second maxillae (trignathous). In fact, monognathous forms have never been found (living or fossilized), but the dignathous condition occurs in Pauropoda and Diplopoda, and trignathous mouthparts are found in centipedes, symphylans, and all hexapods (including insects and their close relatives).
The symphylans and the hexapods (but not the centipedes) have experienced an anatomical fusion of the second maxillae. This medial fusion of the left and right side appendage has produced a mouthpart called the labium. It is tempting to interpret this structural similarity as evidence of a close evolutionary affinity between Symphyla and Insecta. In fact, this was the basis for the "symphylan theory" of insect evolution that was proposed by Calman and Imms in 1936. Despite its intuitive appeal, the "symphylan theory" is not widely accepted today because of other, more extensive differences in leg and abdominal structure between these two groups.
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