vertebrate-life-9th-edition-by-pough-f-harveypdf [78-83].pdf

Ancestral agnathous condition 1st gill slit Braincase 1st gill arch (a) 2nd gill arch Gnathostome condition Lateral view Palatoquadrate (upper jaw = 1st gill arch) Spiracle (= 1st gill slit) Anterior view (form of gill arches 3-7) Pharyngeobranchial Notochord Pharyngeobranchial Epibranchial Ceratobr...

Ancestral agnathous condition 1st gill slit Braincase 1st gill arch (a) 2nd gill arch Gnathostome condition Lateral view Palatoquadrate (upper jaw = 1st gill arch) Spiracle (= 1st gill slit) Anterior view (form of gill arches 3-7) Pharyngeobranchial Notochord Pharyngeobranchial Epibranchial Ceratobranchial Epibranchial Hypobranchial Ceratobranchial Mandible (lower jaw = 1st gill arch) (b) Hyoid arch (= 2nd gill arch) Hypobranchial Basibranchial Basibranchial Figure 3–12 Evolution of the vertebrate jaw from anterior branchial arches. Colored shading indicates splanchnocranium elements (branchial arches and their derivatives). jaws as shown in Figure 3-12(a). However, all vertebrates have some structure in this position (i.e., in the second head segment) that appears to represent the modification of an anterior pair of pharyngeal arches; these are the jaws in gnathostomes and velar cartilages (i.e., the structures that support the velum) in lampreys and hagfishes. Thus it has been proposed that the common ancestor of living vertebrates had an unmodified pair of branchial arches in this position, with a fully functional gill slit lying between the first and second arches, and that living jawless and jawed vertebrates are both divergently specialized from this condition. There is no trace of a gill slit between arches 1 and 2 in living jawless vertebrates; but, in many living cartilaginous fishes, and in a few bony fishes, there is a small hole called the spiracle in this position, which is now used for water intake. Figure 3–12 summarizes the differences in the gill arches between jawed vertebrates and their presumed jawless ancestor and illustrates the major components of the hinged gnathostome gill arches (as seen in arches 3 through 7). Evolution of Gills of Early Vertebrates Because ostracoderms are now viewed as “stem gnathostomes,” any understanding of the origin of gnathostomes must encompass the view that at some point a jawless vertebrate was transformed into a jawed one. However, for much of the last century, researchers considered jawless and jawed vertebrates as two separate evolutionary radiations. This was because of the apparent nonhomology of their branchial arches: at least in living jawless vertebrates (the situation is less clear for the fossil ones), the gill arches lie lateral to (that is, external to) the gill structures, whereas in jawed vertebrates they lie medially (internal to the gills). Additionally, extant jawless vertebrates have pouched gills with small, circular openings that are different from the flatter, more lens-shaped openings between the gills of gnathostomes. However, in the early twenty-first century a veritable explosion of studies on vertebrate head development (especially studies of lampreys) showed that this difference in gill arch position may be produced simply by a switch in developmental timing. The Transition from Jawless to Jawed Vertebrates 63 In addition, hagfishes and lampreys both have some evidence of internal branchial elements in the form of velar cartilages, and some living sharks have evidence of small external branchial cartilages. That observation raises the possibility that the earliest vertebrates may have had both internal and external gill arches, and that is a condition from which both the cyclostome and gnathostome conditions could be derived. The external branchial basket of lampreys, which squeezes the pharyngeal area from the outside, may be essential for the specialized tidal ventilation of adult lampreys. In contrast, the strengthened (and jointed) internal branchial arches in gnathostomes may be related to the more powerful mode of gill ventilation used by these vertebrates. In any event, the difference in gill skeletons that was once thought to be an insurmountable problem for evolving jawed vertebrates from jawless ones is now inconsequential. However, there is one aspect of the agnathan anatomy that did need to change before jaws could develop: the nasohypophyseal duct (see Figure 3–6b) that connects to the pituitary in the brain. In lampreys this duct obstructs the lateral growth of the neuralcrest tissue that forms the gnathostome jaw, so this connection had to be broken before jaws could evolve. In gnathostomes the paired olfactory sacs are widely separated and no longer connect to the hypophyseal pouch. This separation has now been identified in a derived ostracoderm, one of the galeaspids. Thus, the rearrangement of cranial anatomy necessary for jaw evolution was acquired in jawless fishes closely related to gnathostomes. Stages in the Origin of Jaws In recent years, molecular developmental biology has provided fresh insights into the issue of the origin of jaws. It is worth noting that some of the controversies described above relate to a couple of misconceptions about the probable processes of evolution: First, we should consider that evolutionary transformation does not involve changing one adult structure into another adult structure; instead, morphology is altered via modifications of gene expression and shifts in developmental timing. Second, the fact that the lamprey lies below the position of gnathostomes on the cladogram does not mean that it represents a basal vertebrate condition. On the contrary, lampreys, with their bizarrely hypertrophied upper lip, are highly derived in their own right. The same genes are expressed in the mandibular segments of lampreys and gnathostomes, indicating that 64 CHAPTER 3 the structures in this position are likely to be homologous. The lamprey velum and velar cartilages, composed of mandibular segment tissue, are highly specialized structures, and the lamprey upper lip is a strange mixture of material from the mandibular (second) segment and the premandibular (first) segment. Thus, lampreys clearly do not represent a generalized ancestral condition from which gnathostomes might have been derived. Why Evolve Jaws? Although the complex evolutionary hypotheses about the roles of internal and external branchial arches described above may be valid, a relatively simple change in the direction of the streams of neuralcrest tissue that form the arches could also account for the difference in position of jaws in the adult. What is perhaps of more interest to evolutionary morphologists than how such a shift in branchial arch position could have occurred is the reason why jaws evolved at all. The notion that derived predatory vertebrates should convert gill arches into toothed jaws has been more or less unquestioned for decades. It is a common assumption that jaws are superior devices for feeding, and thus more derived vertebrates were somehow bound to obtain them. However, this simplistic approach does not address the issue of how the evolutionary event might actually have taken place: What use would a protojaw be prior to its full transformation? And even if early vertebrates needed some sort of superior mouth anatomy, why modify a branchial gill-supporting arch, which initially was located some distance behind the mouth opening? Why not just modify the existing cartilages and plates surrounding the mouth? There is nothing about those structures that prevents them from being modified. Quite the contrary, in fact—the living agnathans have specialized oral cartilages, and various ostracoderms apparently had oral plates. Additionally, as we noted earlier, gnathostome teeth must have evolved after jaws evolved, so the first jaws were toothless; and of what use could a toothless jaw be? (A movie entitled Gums wouldn’t sell out a theater.) Jon Mallatt has proposed a novel explanation of the origin of jaws based on the hypothesis that jaws were initially important for gill ventilation rather than predation. Living gnathostomes are more active than jawless vertebrates and have greater metabolic demands, and features of the earliest known ones suggest that this was the condition from the start of their evolutionary history. One derived gnathostome feature associated with such high activity is the powerful mechanism for pumping water over the gills. Gnathostomes have a characteristic series Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates (a) Upper-lip skeleton Upper lip Mouth opening Lower lip Gill opening Hyoid arch Mandibular arch Other branchial arches (b) (c) Otic capsule Upper lip First gill opening Hyoid arch Hyoid arch Enlarged mandibular arch Mandibular arch (d) (e) Spiracle Upper lip First gill opening Hyoid arch Jaw = Mandibular arch Hyoid arch Jaw = Mandibular arch Figure 3–13 Proposed evolution of vertebrate jaws. (a) Jawless gnathostome ancestor. The ‘upper lip skeleton’ is derived from the mandibular arch and is considered to be the precursor of the upper jaw. (b) Early pre-gnathostome with jointed branchial arches. (c) Late pre-gnathostome with enlarged mandibular arch now employed to firmly close mouth during ventilation. (d) Early gnathostome with mandibular arch now used as a feeding jaw. (e) More derived gnathostome (e.g., a shark) with teeth added to jaw. of internal branchial muscles (with cranial nerve innovation) as well as the new, external hypobranchials (with spinal nerve innervation). These muscles not only push water through the pharynx in exhalation but also suck water into the pharynx during inhalation. Gnathostome fishes can generate much stronger suction than agnathans, and powerful suction is also a way to draw food into the mouth. Living agnathans derive a certain amount of suction from their pumping velum, but this pump mostly pushes (rather than sucks) water, and its action is weak. Mallatt proposed that the mandibular branchial arch enlarged into protojaws because it played an essential role in forceful ventilation—rapidly closing and opening the entrance to the mouth (Figure 3–13). During strong exhalation, as the pharynx squeezed water back across the gills, water was kept from exiting via the mouth by bending the mandibular arch sharply shut. Next, during forceful inspiration, the mandibular arch was rapidly straightened to reopen the mouth and allow water to enter. To accommodate the forces of the powerful muscles that bent The Transition from Jawless to Jawed Vertebrates 65 the arch (the adductor mandibulae, modified branchial muscles) and straightened it (the hypobranchial muscles), the mandibular arch enlarged and became more robust. The advantage of using the mandibular arch would be that the muscles controlling it are of the same functional series as the other ventilatory muscles, and their common origin would ensure that all of the muscles were controlled by the same nerve circuits. In contrast, the muscles of the more anterior oral cartilages would not have been coupled with the musculature of the pharyngeal arches. Probably that would not have mattered if feeding had been the original function of jaws, whereas it would matter if the jaws had to coordinate their movements with the pharyngeal arches that were responsible for ventilation. This line of reasoning may explain why the mandibular arch, rather than the more anterior oral cartilages, became the jaws of gnathostomes. 3.7 Extinct Paleozoic Jawed Fishes With jaws that can grasp prey, muscles that produce powerful suction, and other features indicative of higher levels of activity, gnathostomes were able to enter ecological niches unavailable to agnathan vertebrates. We have numerous fossils of the entire bodies of gnathostomes (rather than fragments such as teeth and scales) from Devonian sediments. At this point, gnathostomes can be divided into four distinctive clades: two extinct groups—placoderms and acanthodians, and two groups that survive today—chondrichthyans (cartilaginous fishes) and osteichthyans (bony vertebrates): Placoderms were highly specialized, armored fishes that appear to be basal to other gnathostomes. The acanthodians, or “spiny sharks,” were small, more generalized fishes. Although acanthodians have been traditionally grouped with the bony fishes, new studies suggest that the different species occupied a diversity of positions in the vertebrate phylogeny. The cartilaginous fishes, which include sharks, rays, and ratfishes, evolved distinctive specializations of small dermal scales, internal calcification, jaw and fin mobility, and reproduction. Bony fishes evolved endochondral bone in their internal skeleton, a distinctive dermal head skeleton that included an operculum covering the gills, and an internal air sac forming a lung or a swim bladder. The bony fishes include the ray-finned fishes (actinopterygians), which comprise the majority of living fishes, and the lobe-finned fishes (sarcopterygians). 66 CHAPTER 3 Only a few lobe-finned fishes survive today (lungfishes and coelacanths), but they were more diverse in the Paleozoic. (Furthermore, sarcopterygian fishes are the group that gave rise to the tetrapods, and from this perspective there are as many extant species of sarcopterygians as of actinopterygians.) If we take another step back, Osteichthyes includes tetrapods, and we are ourselves highly modified fishes. Bony fishes by themselves constitute a paraphyletic group because their common ancestor is also the ancestor of tetrapods, and the same is true of the lobe-finned fishes. Before studying the extant groups of jawed fishes, we turn to the placoderms and acanthodians to examine the variety of early gnathostomes. Figures 3–3 and 3–4 show the interrelationships of gnathostome fishes. Living and extinct groups of chondrichthyans are discussed in Chapter 5, and osteichthyans are discussed in Chapter 6. Placoderms—The Armored Fishes As the name placoderm (Greek placo = plate and derm = skin) implies, placoderms were covered with a thick bony shield over the anterior one-third to one-half of their bodies. Unlike the ostracoderms, the bony shield of placoderms was divided into separate head and trunk portions, linked by a mobile joint that allowed the head to be lifted up during feeding (Figure 3–14a). The endoskeleton was mineralized by perichondral bone ossification around the rim of the bone (perichondral bone). (Ossification throughout the entire bone [endochondral bone] appears to be limited to osteichthyans.) Many (though not all) researchers consider that placoderms are not a distinctive clade, but rather represent a paraphyletic assemblage at the stem of gnathostome evolution. This would mean that some placoderm species were more closely related to the living groups of gnathostomes than were others. History of Placoderms Placoderms are known from the Early Silurian to the end of the Devonian and were the most diverse vertebrates of their time in terms of number of species, types of morphological specializations, and body sizes, with the largest reaching a length of 8 meters, the size of a great white shark. Like the ostracoderms, they suffered massive losses in the Late Devonian extinctions; but, unlike any ostracoderm group, a few placoderm lineages continued for another 5 million years, until the very end of the period. Ancestral placoderms were primarily marine, but a great many lineages became adapted to freshwater and estuarine habitats. Biology of Placoderms Placoderms have no modern analogues, and their massive external armor makes Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates (a) The arthrodire placoderm Coccosteus Head/trunk joint Lateral view Dorsal view 50 mm Frontal view 50 mm Tooth plates (b) The antiarch placoderm Bothriolepis Pectoral fins encased in armor (c) The giant Late Devonian arthrodire placoderm Dunkleosteus 20 mm (d) The Early Devonian Climatius, a generalized acanthodian Pectoral spine Branchiostegal rays 200 mm 20 mm Pelvic spine Anal spine Intermediate spines Figure 3–14 Extinct Paleozoic fishes: placoderms and acanthodians. interpreting their lifestyle difficult, although they were apparently primarily inhabitants of deep water. Most placoderms lacked true teeth; their toothlike structures (tooth plates, see Figure 3–14a) were actually projections of the dermal jawbones that were subject to wear and breakage without replacement. However, some later placoderms did possess true teeth, possibly evolved convergently with teeth of other gnathostomes. It is impossible to know whether placoderms had many of the soft-anatomy characters of living gnathostomes, but it has been determined that, like their extant relatives, they had myelinated nerve sheaths. Structures preserved in one placoderm were initially interpreted as being lungs, but this notion has now been disproved: these supposed “lungs” appear to be portions of the digestive tract that were filled with sediment after death. More than half of the known placoderms, nearly 200 genera, belonged to the predatory arthrodires (Greek arthros = a joint and dira = the neck). As their Extinct Paleozoic Jawed Fishes 67 name suggests, they had specializations of the joint between the head shield and the trunk shield, allowing an enormous head-up gape, probably increasing both predatory and respiratory efficiency. There was a large diversity of placoderms, many of them flattened, bottom-dwelling forms, some even resembling modernday skates and rays. The antiarchs, such as Bothriolepis, looked rather like armored catfishes (Figure 3–14b). Their pectoral fins were also encased in the bony shield, so that their front fins looked more like those of a crab. Perhaps the best-known placoderm is Dunkleosteus, a voracious, 8-meter-long predatory arthrodire (Figure 3–14c); biomechanical studies have shown that this fish had an extraordinarily powerful bite and rapid gape expansion for suction of prey items. A recent study of placoderms from the Late Devonian of Australia that preserve some soft-tissue structure has provided much more information about these fishes. For example, one way in which they are less derived than other gnathostomes is that their segmental muscles (myomeres) resemble those of lampreys in being only weakly W-shaped and not distinctly separated into epaxial and hypaxial portions. Perhaps the most interesting finding was evidence in one form, appropriately named Materpiscis (Latin mater = mother and piscis = fish), that had embryos and a structure interpreted as an umbilical cord preserved within the body cavity. This evidence of viviparity in at least some placoderms matches the observation that some placoderms also have claspers on their pelvic fins, resembling the pelvic claspers in male modern cartilaginous fishes that are used for internal fertilization (see Chapter 5). We can infer from this that the placoderms, like living chondrichthyans, had internal fertilization and probably complex courtship behaviors. Acanthodians Acanthodians are so named because of the stout spines (Greek acantha = spine) anterior to their well-developed dorsal, anal, and paired fins. Most researchers now consider these fishes to be an array of early forms, some of which were more closely related to the Osteichthyes, others to the Chondrichthyes, and still others perhaps less derived than any extant gnathostome. A recent analysis of Acanthodes indicates that the form of the chondrichthyan braincase is basal for gnathostomes. History of Acanthodians Acanthodians lived from the Late Ordovician through the Early Permian periods, with their major diversity in the Early Devonian. The earliest forms were marine, but by the Devonian they were predominantly a freshwater group. Acanthodians had a basic fusiform fish shape with a heterocercal tail fin (i.e., with the upper lobe larger than the lower lobe; Figure 3–14d). This tail shape in modern fishes is associated with living in the water column, rather than being bottom-dwelling like the placoderms. Biology of Acanthodians Acanthodians were usually not more than 20 centimeters long, although some species reached lengths of 2 meters. They had paired fins, lots of them—some species had as many as six pairs of ventrolateral fins in addition to the pectoral and pelvic fins that gnathostomes have (see Figure 3–14d). Most acanthodians had large heads with wide-gaping mouths, and the teeth (in the species that had teeth—some species were toothless) formed a sharklike tooth whorl. The acanthodids, the only group to survive into the Permian, were elongate, toothless, and with long gill rakers. They were probably plankton-eating filter feeders. Summary Fossil evidence indicates that vertebrates evolved in a marine environment. Jawless vertebrates are first known from the Early Cambrian, and there is evidence that the first jawed vertebrates (gnathostomes) evolved as long ago as the Middle Ordovician. The first vertebrates would have been more active than their ancestors, with a switch from filter feeding to more active predation and with a muscular pharyngeal pump for gill ventilation. The first mineralized tissues were seen in the teeth of conodonts, enigmatic animals that have only recently been considered true vertebrates. Bone is a feature of many early vertebrates, although it was absent from the Early Cambrian forms and is also absent in the living jawless vertebrates—the hagfishes 68 CHAPTER 3 and lampreys. Bone is first found with accompanying external layers of dentine and enamel-like tissue in the dermal armor of early jawless fishes called the ostracoderms. Current explanations for the original evolutionary use of bone include protection, a store for calcium and phosphorus, and housing for electroreceptive sense organs. Among the living jawless fishes, hagfishes are apparently less derived in their anatomy than the lampreys and all other known vertebrates, but molecular data now suggest that they form a clade with lampreys, which would mean that the apparently ancestral anatomical features represent secondary loss of derived characters. Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates