Vertebrate Life PDF

Female lampreys produce hundreds to thousands of eggs, about a millimeter in diameter and devoid of any specialized covering such as that found in hagfishes. Male and female lampreys construct a nest by attaching themselves by their mouths to large rocks and thrashing about violently. Smaller rocks...

Female lampreys produce hundreds to thousands of eggs, about a millimeter in diameter and devoid of any specialized covering such as that found in hagfishes. Male and female lampreys construct a nest by attaching themselves by their mouths to large rocks and thrashing about violently. Smaller rocks are dislodged and carried away by the current. The nest is complete when a pit is rimmed upstream by large stones, downstream by a mound of smaller stones and sand that produces eddies. Water in the nest is oxygenated by this turbulence but does not flow strongly in a single direction. The female attaches to one of the upstream rocks, laying eggs, and the male wraps around her, fertilizing the eggs as they are extruded, a process that may take two days. Adult lampreys die after breeding once. The larvae hatch in about two weeks. The larvae are radically different from their parents and were originally described as a distinct genus, Ammocoetes (see Figure 3–6c). This name has been retained as a vernacular name for the larval form. A week to ten days after hatching, the tiny 6- to 10-millimeter-long ammocoetes leave the nest. They are wormlike organisms with a large, fleshy oral hood and nonfunctional eyes hidden deep beneath the skin. Currents carry the ammocoetes downstream to backwaters and quiet banks, where they burrow into the soft mud or sand and spend three to seven years as sedentary filter feeders. The protruding oral hood funnels water through the muscular pharynx, where food particles are trapped in mucus and carried to the esophagus. An ammocoete may spend its entire larval life in the same bed of sediment, with no major morphological or behavioral change until it is 10 centimeters or longer and several years old. Adult life is usually no more than two years, and many lampreys return to spawn after one year. Lampreys and Humans During the past hundred years, humans and lampreys have increasingly been at odds. Although the sea lamprey, Petromyzon marinus, seems to have been indigenous to Lake Ontario, it was unknown from the other Great Lakes of North America before 1921. From the 1920s to the 1950s, lampreys expanded rapidly across the entire Great Lakes basin, and by 1946 they inhabited all the Great Lakes. Lampreys were able to expand unchecked until sporting and commercial interests became alarmed at the reduction of economically important fish species, such as lake trout, burbot, and lake whitefish. Chemical lampricides as well as electrical barriers and mechanical weirs at the mouths of spawning streams 56 CHAPTER 3 have been employed to bring the Great Lakes lamprey populations down to their present level. 3.3 The Importance of Extant Jawless Vertebrates in Understanding Ancient Vertebrates The fossil record of the first vertebrates reveals little about their pre-Silurian evolution, and it yields no undisputed clues about the evolution of vertebrate structure from the condition in nonvertebrate chordates. Hagfishes and lampreys may provide examples of the early agnathous radiation, but do hagfishes really represent a less derived type of vertebrate than the lamprey? This question is important for understanding the biology of the first vertebrates: Were the first vertebrates as lacking in derived characters as living hagfishes appear to be, or were they somewhat more complex animals? Anatomical Evidence On balance, anatomical features of hagfishes appear to represent a more ancestral condition than those in lampreys, but the interpretation of many of these features is controversial. Some aspects of the anatomy of hagfishes, notably aspects of the brain and neuroanatomy, do appear to be truly ancestral. Other apparently basal features, such as the rudimentary eyes, may represent a secondary loss of more derived characters. Some characters, such as the very simple kidney, the lack of innervation of the heart (and the presence of amphioxus-like accessory hearts), and the body fluids that are the same concentration as seawater, are simply hard to interpret. Molecular Evidence The majority of molecular studies link hagfishes and lampreys as sister taxa, but we cannot get molecules from early nonvertebrate chordates (such as the Cambrian Haikouella) or from early vertebrates (such as the Cambrian vertebrate Haikouichthys and the huge diversity of ostracoderms) for comparison. Missing data of this sort can bias the computer programs that create phylogenies by introducing a statistical artifact known as “long branch attraction” that does not represent the true phylogenetic relationship. We do not Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates claim here that the molecular findings in the case of lampreys and hagfishes are artifacts, but the difference in the results obtained from morphological data versus molecular data is troubling. Recent molecular studies have focused on small portions of the genome called microRNAs, which are particularly prominent in vertebrates, and which appear to have been accumulating in vertebrate genomes over time (see Chapter 2). Studies of hagfishes and lampreys show that these two types of cyclostomes have four unique families of microRNAs, suggesting that they are in fact closely related. However, microRNAs apparently may be lost over time, so the debate is likely to continue. 3.4 The Radiation of Paleozoic Jawless Vertebrates— “Ostracoderms” “Ostracoderms” is a paraphyletic assemblage because some more derived types of ostracoderms are clearly more closely related to the gnathostomes (jawed vertebrates) than others (see Figure 3–3). Our interpretation of exactly how different lineages of ostracoderms are related to one another and to living vertebrates has changed considerably since the latter part of the twentieth century. Ostracoderms are clearly more derived than extant agnathans: Ostracoderms had dermal bone, and impressions on the underside of the dorsal head shield suggest that they had derived (i.e., gnathostome-like) features—a cerebellum in the hindbrain and an olfactory tract connecting the olfactory bulb with the forebrain. (Living agnathans lack a distinct cerebellum, and their olfactory bulbs are incorporated within the rest of the forebrain rather than placed more anteriorly and linked to the head via the olfactory tract [cranial nerve I].) Characters of Ostracoderms Most ostracoderms are characterized by the presence of a covering of dermal bone, usually in the form of an extensive armored shell, or carapace, but sometimes in the form of smaller plates or scales (e.g., anaspids), and some are relatively naked (e.g., thelodonts). Ostracoderms ranged in length from about 10 centimeters to more than 50 centimeters. Although they lacked jaws, some apparently had various types of movable mouth plates that have no analogues in any living vertebrates. These plates were arranged around a small, circular mouth that appears to have been located farther forward in the head than the larger, more gaping mouth of jawed vertebrates. Most species of ostracoderms probably ate small, soft-bodied prey. Most ostracoderms had some sort of midline dorsal fin, and although many heterostracans and anaspids had some sort of anterior, paired, finlike projections, only the more derived osteostracans had true pectoral fins, with an accompanying pectoral girdle and endoskeletal fin supports. As in living jawless vertebrates, the notochord must have been the main axial support throughout adult life. Figure 3–7 depicts some typical ostracoderms. Agnathans and Gnathostomes During the Late Silurian and the Devonian, most major known groups of extinct agnathans coexisted with early gnathostomes, and it is highly unlikely that ostracoderms were pushed into extinction by the radiation of gnathostomes after 50 million years of coexistence. Jawless and jawed vertebrates appear to represent two different basic types of animals that probably exploited different types of resources. The initial reduction of ostracoderm diversity at the end of the Early Devonian may be related to a lowering of global sea levels, with the resulting loss of coastal marine habitats. The extinction of the ostracoderms in the Late Devonian occurred at the same time as mass extinctions among many marine invertebrates, which suggests that their demise was not due to gnathostome competition. Gnathostomes also suffered in the Late Devonian mass extinctions, and the placoderm lineage that dominated the Devonian period became extinct at its end. 3.5 The Basic Gnathostome Body Plan Gnathostomes are considerably more derived than agnathans, not only in their possession of jaws but also in many other ways. Jaws allow a variety of new feeding behaviors, including the ability to grasp objects firmly, and along with teeth enable the animal to cut food to pieces small enough to swallow or to grind hard foods. New food resources became available when vertebrates evolved jaws: Herbivory was now possible, as was taking bite-sized pieces from large prey items, and many gnathostomes became larger than contemporary jawless vertebrates. A grasping, movable jaw also permits manipulation of objects: The Basic Gnathostome Body Plan 57 The heterostracan Pteraspis (Pteraspida) (Late Silurian) Mouth The psammosteid heterostracan (Pteraspida) Drepanaspis (dorsal view) (Early Devonian) 10 mm Gill opening Hypocercal tail (a) Gill opening Mouth (b) The anaspid Pharyngolepis (Cephalaspida) (Late Silurian) 10 mm Eye Orbital plate Hypocercal tail Gill openings (c) Lateral spine 10 mm Anal spine Late Silurian thelodonts Phlebolepis (d) 10 mm The osteostracan Hemicyclaspis (Cephalaspida) (Late Devonian) Loganellia (a fork-tail) Dorsal scales = anterior dorsal fin Posterior dorsal fin 10 mm Heterocercal tail Galeaspid (Cephalaspida) from the Early Devonian Hypochordal lobe ? sensory field area Ventrolateral ridge (e) Pectoral fin 10 mm Pituriaspid (Cephalaspida) from the Devonian (f) (g) 58 CHAPTER 3 10 mm Figure 3–7 Ostracoderm diversity: Pteraspida and common Cephalaspida. Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates jaws are used to dig holes, to carry pebbles and vegetation to build nests, and to grasp mates during courtship and juveniles during parental care. However, it seems that the likely origin of jaws was for more efficient gill ventilation rather than predation, as will be discussed later. Gnathostome Biology Gnathostomes are first known with certainty from the Early Silurian, but isolated sharklike scales suggest that they date back to the Middle Ordovician. The difference between gnathostomes and agnathans is traditionally described as the presence of jaws that bear teeth and two sets of paired fins or limbs (pectoral and pelvic). However, the gnathostome body plan (Figure 3–8) reveals that they are characterized by many other features, implying that gnathostomes represent a basic step up in level of activity and complexity from the jawless vertebrates. Interestingly, the form of the gnathostome lower jaw seems to be most variable in 9 Nerve cord 5 6 Dorsal fin the Silurian, when jawed fishes were not very common. By the Devonian, when the major radiation of jawed vertebrates commenced, the variety of jaw forms had stabilized. These derived features include improvements in locomotor and predatory abilities and in the sensory and circulatory systems. Just as jawless vertebrates show a duplication of the Hox gene complex in comparison to nonvertebrate chordates (see Chapter 2), living jawed vertebrates show evidence of a second Hox duplication event. Gene duplication would have resulted in a greater amount of genetic information, perhaps necessary for building a more complex type of animal. However, as can be seen in Figure 3–3, a number of extinct ostracoderm taxa lie between living agnathans and gnathostomes, and many features seen today only in gnathostomes might have been acquired in a steplike fashion throughout ostracoderm evolution. Paired pectoral fins, for example, are usually considered to be a gnathostome character, but some osteostracans had evolved paired fins. Segmental axial muscles Neural arch Notochord 4 Hemal arch 1 2 3 8 7 Caudal fin Anal fin Pelvic fins Pectoral fins Figure 3–8 Generalized jawed vertebrate (gnathostome) showing derived features compared to the jawless vertebrate (agnathan) condition. Legend: 1. Jaws (containing teeth) formed from the mandibular gill arch. 2. Gill skeleton consists of jointed branchial arches and contains internal gill rakers that stop particulate food from entering the gills. Gill musculature is also more robust. 3. Hypobranchial musculature allows strong suction in inhalation and suction feeding. 4. Two distinct olfactory tracts, leading to two distinct nostrils. 5. Original first gill slit squeezed to form the spiracle, situated between the mandibular and hyoid arches. 6. Three semicircular canals in the inner ear (addition of horizontal canal). 7. Addition of a conus arteriosus to the heart, between the ventricle and the ventral aorta. (Note that the position of the heart is actually more anterior than shown here, right behind the most posterior gill arch.) 8. Horizontal septum divides the trunk muscle into epaxial (dorsal) and hypaxial (ventral) portions. It also marks the position of the lateral line canal, containing the neuromast sensory organs. 9. Vertebrae now have centra (elements surrounding the notochord) and ribs, but note that the earliest gnathostomes have only neural and hemal arches, as shown in the posterior trunk. The Basic Gnathostome Body Plan 59 Jaws and Teeth Extant gnathostomes have teeth on their jaws, but teeth must have evolved after the jaws were in place because early members of the most basal group of jawed fishes—the placoderms—appear to have lacked true teeth (see section 3.6). Another reason to dissociate the evolution of jaws from the evolution of teeth is the presence of pharyngeal toothlike structures in various jawless vertebrates. These are most notable in the conodonts previously discussed (see Figure 3–2) but also have been reported in thelodonts, which are poorly known ostracoderms that lack a well-mineralized skeleton. Developmental studies support the notion that the first teeth were not oral structures but were located in the pharynx. Bony fishes and tetrapods have teeth embedded in the jawbones (Figure 3–9). However, because teeth form from a dermal papilla, they can be embedded only in dermal bones, and cartilaginous fishes such as sharks and rays lack dermal bone. The teeth of cartilaginous fishes form within the skin, resulting in a tooth whorl that rests on the jawbone but is not actually embedded in it. This condition is probably the ancestral one for all gnathostomes more derived than placoderms because it is also seen in the extinct acanthodians (see section 3.6). Adding jaws and hypobranchial muscles (which are innervated by spinal nerves) to the existing branchiomeric muscles (innervated by cranial nerves) allowed vertebrates to add powerful suction to their feeding mechanisms (Figure 3–10a). The cranium of gnathostomes has also been elongated both anteriorly and posteriorly compared with the agnathan condition. segmental muscles, providing increased anchorage for axial muscles. There is now a clear distinction between the epaxial and hypaxial blocks of the axial muscles, which are divided by a horizontal septum made of thin fibrous tissue that runs the length of the animal. The lateral line canal—containing the organs that sense vibrations in the surrounding water—lies in the plane of this septum, perhaps Replacement teeth Skin Mandible (a) Tooth whorl Replacement tooth (b) Pleurodont Replacement tooth (c) Acrodont Vertebrate and Ribs Progressively more complex ver- tebrae are another gnathostome feature. Gnathostome vertebrae initially consisted of arches flanking the nerve cord dorsally (the neural arches, which are homologous with the arcualia of lampreys) with matching arches below the notochord (the hemal arches, which may be present in the tail only—see the posterior portion of the trunk in Figure 3–8). More derived gnathostomes had a vertebral centrum or central elements with attached ribs (Figure 3–10b). Still more complete vertebrae support the notochord and eventually replace it as a supporting rod for the axial muscles used for locomotion (mainly in tetrapods). Well-developed centra were not a feature of the earliest jawed fishes and are unknown in the two extinct groups of fishes—placoderms and acanthodians. Ribs are another new feature in gnathostomes. They lie in the connective tissue between successive 60 CHAPTER 3 Replacement tooth (d) Thecodont © 1998 The McGraw-Hill Companies, Inc. Figure 3–9 Gnathostome teeth. (a) Tooth whorl of a chondrichthyan. (b–d) Teeth embedded in the dermal bones of the jaw as seen in osteichthyan fishes and tetrapods. (b) Pleurodont, the basal condition: teeth set in a shelf on the inner side of the jawbone, seen in some bony fishes and in modern amphibians and some lizards. (c) Acrodont condition: teeth fused to the jawbone, seen in most bony fishes and in some reptiles (derived independently). (d) Thecodont condition: teeth set in sockets and held in place by peridontal ligaments, seen in archosaurian reptiles and mammals (derived independently). Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates Adductor mandibulae Neural arch Hypobranchials Spinal cord Cucullaris Notochord Pectoral-fin elevator Centrum elements Rib (b) Ventral constrictors Branchiomeric muscle (cranially innervated) Pectoral fin depressor Spinally innervated muscles (a) Figure 3–10 Some gnathostome specializations. (a) Ventral view of a dogfish, showing both branchiomeric muscles and the new, spinally innervated, hypobranchial muscles. (b) View of generalized gnathostome vertebral form, showing central elements and ribs. reflecting improved integration between locomotion and sensory feedback. In the inner ear there is a third (horizontal) semicircular canal, which may reflect an improved ability to navigate and orient in three dimensions. What About Soft Tissues? Features such as jaws and ribs can be observed in fossils, so we know that they are unique to gnathostomes. However, we cannot know for sure whether other new features within the soft anatomy characterize gnathostomes alone or whether they were adopted somewhere within the ostracoderm lineage. We can surmise that some features of the nervous system that are seen only in gnathostomes among living vertebrates were acquired by the earliest ostracoderms. For example, impressions on the inner surface of the dermal head shield reveal the presence of a cerebellum in the brain and olfactory tracts. We can see that no ostracoderm possessed a third semicircular canal. A new feature of the nervous system in gnathostomes is the insulating sheaths of myelin on the nerve fibers, which increase the speed of nerve impulses. The heart of gnathostomes has an additional small chamber in front of the pumping ventricle, the conus arteriosus, which acts as an elastic reservoir that smoothes out the pulsatile nature of the flow of blood produced by contractions of a more powerful heart. (Some workers consider that lampreys, but not hagfishes, have a small conus arteriosus despite their weak hearts and low blood pressures.) Living agnathans lack a stomach, but some derived ostracoderms may have had a stomach. Gnathostomes also have a type of cartilage different from the cartilage seen in the hagfishes and lampreys. (See Chapter 2 and the legend to Figure 3–3 in the Appendix for additional gnathostome characters.) One particularly important gnathostome feature is in the reproductive system, where the gonads now have their own specialized ducts leading to the cloaca (see Chapter 2). The Origin of Fins Guidance of a body in three-dimensional space is complicated. Fins act as hydrofoils, applying pressure to the surrounding water. Because water is practically incompressible, force applied by a fin in one direction against the water produces a thrust in the opposite direction. A tail fin increases the area of the tail, giving more thrust during propulsion, and allows the fin to exert the force needed for rapid acceleration. Rapid adjustments of the body position in the water may be The Basic Gnathostome Body Plan 61 Pitch Pitch Yaw Roll Yaw Figure 3–11 An early jawed fish (the acanthodian, Climatius). Views from the side and front illustrate pitch, yaw, and roll and the fins that counteract these movements. especially important for active, predatory fishes such as the early gnathostomes, and the unpaired fins in the midline of the body (the dorsal and anal fins) control the tendency of a fish to roll (rotate around the body axis) or yaw (swing to the right or left) (Figure 3–11). The paired fins (pectoral and pelvic fins) can control the pitch (tilt the fish up or down) and act as brakes, and they are occasionally specialized to provide thrust during swimming, like the enlarged pectoral fins of skates and rays. The basic form of the pectoral and pelvic fins, as seen today in chondrichthyans and basal bony fishes, is for a tribasal condition. This means that three main elements within the fin articulate with the limb girdle within the body, and molecular studies back up the anatomical ones in showing that this type of fin represents the ancestral gnathostome condition. The paired fins of gnathostomes also share patterns of development, involving particular Hox genes, with the median fins of lampreys. Fins have non-locomotor functions as well. Spiny fins are used in defense, and they may become systems to inject poison when combined with glandular secretions. Colorful fins are used to send visual signals to potential mates, rivals, and predators. Even before the gnathostomes appeared, fishes had structures that served the same purpose as fins. Many ostracoderms had spines or enlarged scales derived from dermal armor that acted like immobile fins. Some anaspids had long finlike sheets of tissue running along the flanks, and osteostracans had pectoral fins. 62 CHAPTER 3 3.6 The Transition from Jawless to Jawed Vertebrates In Chapter 2 we saw that the branchial arches were a fundamental feature of the vertebrate cranium, providing support for the gills. It has long been known that vertebrate jaws are made of the same material as the skeletal elements that support the gills (cartilage derived from the neural crest), and they clearly develop from the first (mandibular) arch of this series in vertebrates. (Note that while the word “mandible” commonly refers to the lower jaw only, the term “mandibular arch” includes both upper and lower jaws.) It is helpful at this stage to envisage the vertebrate head as a segmented structure, with each branchial arch corresponding to a segment (Figure 3–12). The mandibular arch that forms the gnathostome jaw is formed within the second head segment; jaw supports are formed from the hyoid arch of the third head segment; and the more posterior branchial arches that form the gill supports (arches 3 through 7) are formed in head segments 4 through 8. The branchial arch numbering does not match the numbering of the head segments because no evidence exists for a branchial arch functioning as a gill support structure in the first (premandibular) segment at any point in vertebrate history. No living vertebrate has a pair of gill-supporting branchial arches in such an anterior position as the Early Vertebrates: Jawless Vertebrates and the Origin of Jawed Vertebrates