Vertebrate

Fossilized skeleton (cast) of Diplodocus carnegii, showing an extreme example of the backbone that characterizes the vertebrates.

With only one exception, the defining characteristic of a vertebrate is the vertebral column, in which the embryonic notochord found in all chordates is replaced by a segmented series of mineralized elements called vertebrae separated by fibrocartilaginous intervertebral discs, which are derived embryonically and evolutionarily from the notochord. Hagfish are the only extant vertebrate whose notochord is not integrated into the vertebral column.

A few vertebrates have secondarily lost this feature and retain the notochord into adulthood, such as the sturgeon[14] and coelacanth. Jawed vertebrates are typified by paired appendages (fins or limbs, which may be secondarily lost), but this trait is not required to qualify an animal as a vertebrate.

Gill arches bearing gills in a pike

All basal vertebrates are aquatic and breathe with gills. The gills are carried right behind the head, bordering the posterior margins of a series of openings from the pharynx to the exterior. Each gill is supported by a cartilaginous or bony gill arch.[15] The bony fish have three pairs of arches, cartilaginous fish have five to seven pairs, while the primitive jawless fish have seven. The vertebrate ancestor no doubt had more arches than this, as some of their chordate relatives have more than 50 pairs of gills.[13] In jawed vertebrates, the first gill arch pair evolved into the jointed jaws and form an additional oral cavity ahead of the pharynx.

In amphibians and some primitive bony fishes, the larvae bear external gills, branching off from the gill arches.[16] These are reduced in adulthood, their function taken over by the gills proper in fishes and by lungs in most amphibians. Some amphibians retain the external larval gills in adulthood, the complex internal gill system as seen in fish apparently being irrevocably lost very early in the evolution of tetrapods.[17]

While the more derived vertebrates lack gills, the gill arches form during fetal development, and form the basis of essential structures such as jaws, the thyroid gland, the larynx, the columella (corresponding to the stapes in mammals) and, in mammals, the malleus and incus.[13]

The central nervous system of vertebrates is based on the hollow dorsal nerve cord running along the dorsal aspect of the notochord. Of particular importance and unique to vertebrates is the presence of neural crest cells, which are progenitor cells critical to coordinating the functions of cellular components.[18] Neural crest cells migrate through the body from the nerve cord during development, and initiate the formation of neural ganglia and structures such as the jaws and skull.[19][20][21] The peripheral nervous system forms when neural crest cells branch out laterally from the dorsal nerve cord and migrate together with the mesodermal somites to innervate the various different structures that develop in the body.

The vertebrates are the only chordate group with neural cephalization, and their neural functions are centralized towards a series of vesicular enlargements in the head, which give rise to a brain. A slight swelling of the anterior end of the nerve cord is found in invertebrate chordates such as lancelets (a sister subphylum known as the cephalochordates), though it lacks eyes and other complex special sense organs comparable to those of vertebrates. Other chordates do not show any trends towards cephalization.[13]

The rostral end of the neural tube is expanded by a thickening of the walls and expansion of the central canal of spinal cord into three primary brain vesicles: the prosencephalon (forebrain), mesencephalon (midbrain) and rhombencephalon (hindbrain), which are further differentiated in the various vertebrate groups.[22] Two laterally placed retinas and optical nerves form around outgrowths from the midbrain, except in hagfish, though this may be a secondary loss.[23][24] The forebrain is more well-developed in most tetrapods and subdivided into the telencephalon and diencephalon, while the midbrain dominates in many fish and some salamanders. Vesicles of the brain are usually bilaterally symmetrical, giving rise to the paired cerebral hemispheres in mammals.[22]

The resulting anatomy of the central nervous system with a single hollow nerve cord dorsal to the gut tube, headed by a series of (often paired) vesicles, is unique to vertebrates. Other invertebrates with well-developed central nervous systems such as arthropods and cephalopods, have a ventral nerve cord made of segmental ganglia on the opposite side of the gut tube, with a split brain stem circumventing the foregut around each side to form a brain on the dorsal side of the mouth.[13]

Originally, the "Notochordata hypothesis" suggested that the Cephalochordata is the sister taxon to Craniata (Vertebrata). This group, called the Notochordata, was placed as sister group to the Tunicata (Urochordata). Although this was once the leading hypothesis,[26] studies since 2006 analyzing large sequencing datasets strongly support Olfactores (tunicates + vertebrates) as a monophyletic clade,[27][28][25] and the placement of Cephalochordata as sister-group to Olfactores (known as the "Olfactores hypothesis"). As chordates, they all share the presence of a notochord, at least during a stage of their life cycle.

The following cladogram summarizes the systematic relationships between the Olfactores (vertebrates and tunicates) and the Cephalochordata.

The early vertebrate Haikouichthys

Vertebrates originated during the Cambrian explosion, which saw a rise in organism diversity. The earliest known vertebrates belongs to the Chengjiang biota[29] and lived about 518 million years ago.[1] These include Haikouichthys, Myllokunmingia,[29] Zhongjianichthys,[30] and probably Haikouella.[31] Unlike the other fauna that dominated the Cambrian, these groups had the basic vertebrate body plan: a notochord, rudimentary vertebrae, and a well-defined head and tail.[32] All of these early vertebrates lacked jaws in the common sense and relied on filter feeding close to the seabed.[33] A vertebrate group of uncertain phylogeny, small eel-like conodonts, are known from microfossils of their paired tooth segments from the late Cambrian to the end of the Triassic.[34]

Acanthostega, a fish-like early labyrinthodont.

The first jawed vertebrates may have appeared in the late Ordovician (~445 mya) and became common in the Devonian period, often known as the "Age of Fishes".[35] The two groups of bony fishes, the actinopterygii and sarcopterygii, evolved and became common.[36] The Devonian also saw the demise of virtually all jawless fishes save for lampreys and hagfish, as well as the Placodermi, a group of armoured fish that dominated the entirety of that period since the late Silurian as well as the eurypterids, dominant animals of the preceding Silurian, and the anomalocarids. By the middle of the Devonian, several droughts, anoxic events and oceanic competition lead a lineage of sarcopterygii to leave water, eventually establishing themselves as terrestrial tetrapods in the succeeding Carboniferous.

Amniotes branched from amphibious tetrapods early in the Carboniferous period. The synapsid amniotes were dominant during the late Paleozoic, the Permian, while diapsid amniotes became dominant during the Mesozoic. In the sea, the teleosts and sharks became dominant. Mesothermic synapsids called cynodonts gave rise to endothermic mammals and diapsids called dinosaurs eventually gave rise to endothermic birds, both in the Jurassic.[37] After all dinosaurs except birds went extinct by the end of the Cretaceous, birds and mammals diversified and filled their niches.

The Cenozoic world saw great diversification of bony fishes, amphibians, reptiles, birds and mammals.[38][39]

Over half of all living vertebrate species (about 32,000 species) are fish (non-tetrapod craniates), a diverse set of lineages that inhabit all the world's aquatic ecosystems, from snow minnows (Cypriniformes) in Himalayan lakes at elevations over 4,600 metres (15,100 feet) to flatfishes (order Pleuronectiformes) in the Challenger Deep, the deepest ocean trench at about 11,000 metres (36,000 feet). Many fish varieties are the main predators in most of the world's freshwater and marine water bodies . The rest of the vertebrate species are tetrapods, a single lineage that includes amphibians (with roughly 7,000 species); mammals (with approximately 5,500 species); and reptiles and birds (with about 20,000 species divided evenly between the two classes). Tetrapods comprise the dominant megafauna of most terrestrial environments and also include many partially or fully aquatic groups (e.g., sea snakes, penguins, cetaceans).

Traditional spindle diagram of the evolution of the vertebrates at class level

Conventional classification has living vertebrates grouped into seven classes based on traditional interpretations of gross anatomical and physiological traits. This classification is the one most commonly encountered in school textbooks, overviews, non-specialist, and popular works. The extant vertebrates are:[13]

• Subphylum Vertebrata
  • Class Agnatha (jawless fishes)
  • Class Chondrichthyes (cartilaginous fishes)
  • Class Osteichthyes (bony fishes)
  • Class Amphibia (amphibians)
  • Class Reptilia (reptiles)
  • Class Aves (birds)
  • Class Mammalia (mammals)

In addition to these, there are two classes of extinct armoured fishes, the Placodermi and the Acanthodii, both considered paraphyletic.

Other ways of classifying the vertebrates have been devised, particularly with emphasis on the phylogeny of early amphibians and reptiles. An example based on Janvier (1981, 1997), Shu et al. (2003), and Benton (2004)[42] is given here († = extinct):

Diversity of various groups of vertebrates through the geologic ages. The width of the bubbles signifies the diversity (number of families).

• Subphylum Vertebrata
  • †Palaeospondylus
  • Infraphylum Agnatha or Cephalaspidomorphi (lampreys and other jawless fishes)
    • Superclass †Anaspidomorphi (anaspids and relatives)
  • Infraphylum Gnathostomata (vertebrates with jaws)
    • Class †Placodermi (extinct armoured fishes)
    • Class Chondrichthyes (cartilaginous fishes)
    • Class †Acanthodii (extinct spiny "sharks")
    • Superclass Osteichthyes (bony vertebrates)
      • Class Actinopterygii (ray-finned bony fishes)
      • Class Sarcopterygii (lobe-finned fishes, including the tetrapods)
    • Superclass Tetrapoda (four-limbed vertebrates)
      • Class Amphibia (amphibians, some ancestral to the amniotes)—now a paraphyletic group
      • Class Synapsida (mammals and the extinct mammal-like reptiles)
      • Class Sauropsida (reptiles and birds)

While this traditional classification is orderly, most of the groups are paraphyletic, i.e. do not contain all descendants of the class's common ancestor.[42] For instance, descendants of the first reptiles include modern reptiles, mammals and birds; the agnathans have given rise to the jawed vertebrates; the bony fishes have given rise to the land vertebrates; the traditional "amphibians" have given rise to the reptiles (traditionally including the synapsids or mammal-like "reptiles"), which in turn have given rise to the mammals and birds. Most scientists working with vertebrates use a classification based purely on phylogeny,[43] organized by their known evolutionary history and sometimes disregarding the conventional interpretations of their anatomy and physiology.

In phylogenetic taxonomy, the relationships between animals are not typically divided into ranks but illustrated as a nested "family tree" known as a phylogenetic tree. The cladogram below is based on studies compiled by Philippe Janvier and others for the Tree of Life Web Project and Delsuc et al.,[44][45] and complemented (based on[46],[47] and [48]). A dagger (†) denotes an extinct clade, whereas all other clades have living descendants.

The galeaspid Nochelaspis maeandrine from the Devonian period

The placoderm Dunkleosteus terrelli from the Devonian period

The acanthodian fish Diplacanthus acus from the Devonian period

The early ray-fin Cheirolepis canadensis from the Devonian period

The tetrapodomorph Tiktaalik roseae from the Devonian period

The early tetrapod Seymouria from the Permian period

The synapsid "mammal-like reptile" Dimetrodon limbatus from the Permian period

The bird-like dinosaur Archaeopteryx lithographica from the Jurassic period

Note that, as shown in the cladogram above, the †"Ostracodermi" (armoured jawless fishes) and †"Placodermi" (armoured jawed fishes) are shown to be paraphylectic groups, separated from Gnathostomes and Eugnathostomes respectively.[49][50]

Also note that Teleostei (Neopterygii) and Tetrapoda (amphibians, mammals, reptiles, birds) each make up about 50% of today's vertebrate diversity, while all other groups are either extinct or rare. The next cladogram shows the extant clades of tetrapods (the four-limbed vertebrates), and a selection of extinct (†) groups:

Note that reptile-like amphibians, mammal-like reptiles, and non-avian dinosaurs are all paraphyletic.

The placement of hagfish on the vertebrate tree of life has been controversial. Their lack of proper vertebrae (among with other characteristics found in lampreys and jawed vertebrates) led phylogenetic analyses based on morphology to place them outside Vertebrata. Molecular data, however, indicates they are vertebrates closely related to lampreys. A study by Miyashita et al. (2019), 'reconciliated' the two types of analysis as it supports the Cyclostomata hypothesis using only morphological data.[51]

The following databases maintain (more or less) up-to-date lists of vertebrate species:

• Fish: Fishbase
• Amphibians: Amphibiaweb
• Reptiles: Reptile Database
• Birds: Avibase
• Mammals: Mammal species of the World

During sexual reproduction, mating with a close relative (inbreeding) often leads to inbreeding depression. Inbreeding depression is considered to be largely due to expression of deleterious recessive mutations.[54] The effects of inbreeding have been studied in many vertebrate species.

In several species of fish, inbreeding was found to decrease reproductive success.[55][56][57]

Inbreeding was observed to increase juvenile mortality in 11 small animal species.[58]

A common breeding practice for pet dogs is mating between close relatives (e.g. between half- and full siblings).[59] This practice generally has a negative effect on measures of reproductive success, including decreased litter size and puppy survival.[60][61][62]

Incestuous matings in birds result in severe fitness costs due to inbreeding depression (e.g. reduction in hatchability of eggs and reduced progeny survival).[63][64][65]

As a result of the negative fitness consequences of inbreeding, vertebrate species have evolved mechanisms to avoid inbreeding.

Numerous inbreeding avoidance mechanisms operating prior to mating have been described. Toads and many other amphibians display breeding site fidelity. Individuals that return to natal ponds to breed will likely encounter siblings as potential mates. Although incest is possible, Bufo americanus siblings rarely mate.[66] These toads likely recognize and actively avoid close kin as mates. Advertisement vocalizations by males appear to serve as cues by which females recognize their kin.[66]

Inbreeding avoidance mechanisms can also operate subsequent to copulation. In guppies, a post-copulatory mechanism of inbreeding avoidance occurs based on competition between sperm of rival males for achieving fertilization.[67] In competitions between sperm from an unrelated male and from a full sibling male, a significant bias in paternity towards the unrelated male was observed.[67]

When female sand lizards mate with two or more males, sperm competition within the female's reproductive tract may occur. Active selection of sperm by females appears to occur in a manner that enhances female fitness.[68] On the basis of this selective process, the sperm of males that are more distantly related to the female are preferentially used for fertilization, rather than the sperm of close relatives.[68] This preference may enhance the fitness of progeny by reducing inbreeding depression.

Mating with unrelated or distantly related members of the same species is generally thought to provide the advantage of masking deleterious recessive mutations in progeny[69] (see heterosis). Vertebrates have evolved numerous diverse mechanisms for avoiding close inbreeding and promoting outcrossing[70] (see inbreeding avoidance).

Outcrossing as a way of avoiding inbreeding depression has been especially well studied in birds. For instance, inbreeding depression occurs in the great tit (Parus major) when the offspring are produced as a result of a mating between close relatives. In natural populations of the great tit, inbreeding is avoided by dispersal of individuals from their birthplace, which reduces the chance of mating with a close relative.[71]

Purple-crowned fairywren females paired with related males may undertake extra-pair matings that can reduce the negative effects of inbreeding, despite ecological and demographic constraints.[65]

Southern pied babblers (Turdoides bicolor) appear to avoid inbreeding in two ways: through dispersal and by avoiding familiar group members as mates.[72] Although both genders disperse locally, they move outside the range where genetically related individuals are likely to be encountered. Within their group, individuals only acquire breeding positions when the opposite-sex breeder is unrelated.

Cooperative breeding in birds typically occurs when offspring, usually males, delay dispersal from their natal group in order to remain with the family to help rear younger kin.[73] Female offspring rarely stay at home, dispersing over distances that allow them to breed independently or to join unrelated groups.

Parthenogenesis is a natural form of reproduction in which growth and development of embryos occur without fertilization.

Reproduction in squamate reptiles is ordinarily sexual, with males having a ZZ pair of sex determining chromosomes, and females a ZW pair. However, various species, including the Colombian Rainbow boa (Epicrates maurus), Agkistrodon contortrix (copperhead snake) and Agkistrodon piscivorus (cotton mouth snake) can also reproduce by facultative parthenogenesis—that is, they are capable of switching from a sexual mode of reproduction to an asexual mode—resulting in production of WW female progeny.[74][75] The WW females are likely produced by terminal automixis.

Mole salamanders are an ancient (2.4–3.8 million year-old) unisexual vertebrate lineage.[76] In the polyploid unisexual mole salamander females, a premeiotic endomitotic event doubles the number of chromosomes. As a result, the mature eggs produced subsequent to the two meiotic divisions have the same ploidy as the somatic cells of the female salamander. Synapsis and recombination during meiotic prophase I in these unisexual females is thought to ordinarily occur between identical sister chromosomes and occasionally between homologous chromosomes. Thus little, if any, genetic variation is produced. Recombination between homeologous chromosomes occurs only rarely, if at all.[77] Since production of genetic variation is weak, at best, it is unlikely to provide a benefit sufficient to account for the long-term maintenance of meiosis in these organisms.

Two killifish species, the mangrove killifish (Kryptolebias marmoratus) and Kryptolebias hermaphroditus, are the only known vertebrates to self-fertilize.[78] They produce eggs and sperm by meiosis and routinely reproduce by self-fertilisation. This capacity has apparently persisted for at least several hundred thousand years.[79] Each individual hermaphrodite normally fertilizes itself through uniting inside the fish's body of an egg and a sperm that it has produced by an internal organ.[80] In nature, this mode of reproduction can yield highly homozygous lines composed of individuals so genetically uniform as to be, in effect, identical to one another.[81][82] Although inbreeding, especially in the extreme form of self-fertilization, is ordinarily regarded as detrimental because it leads to expression of deleterious recessive alleles, self-fertilization does provide the benefit of fertilization assurance (reproductive assurance) at each generation.[81]