Synthesis

After summarizing the earlier chapters, which focused on the evolution of specific lineages, this chapter examines general patterns in the evolution of vertebrate nervous systems. Most conspicuous is that relative brain size and complexity increased independently in many lineages. The proportional size of individual brain regions tends to change predictably with absolute brain size (and neurogenesis timing), but the scaling rules vary across lineages. Attempts to link variation in the size of individual brain areas (or entire brains) to behavior are complicated in part because the connections, internal organization, and functions of individual brain regions also vary across phylogeny. In addition, major changes in the functional organization of vertebrate brains were caused by the emergence of novel brain regions (e.g., neocortex in mammals and area dorsalis centralis in teleosts) and novel circuits. These innovations significantly modified the “vertebrate brain Bauplan,” but their mechanistic origins and implications require further investigation.

The Conquest of Land

Early amniotes evolved water-resistant skin and eggs, which allowed them to live and reproduce entirely on land. Roughly 300 million years ago, amniotes split into synapsids (including mammals) and sauropsids (“reptiles” and birds). The sauropsid lineage includes squamates (lizards and snakes), turtles, and archosaurs (crocodilians and dinosaurs, including birds). Tympanic ears and more complex auditory systems evolved at least twice within the various amniote lineages. Amniotes also evolved a separate vomeronasal epithelium and more diverse modes of locomotion and feeding. Brain size relative to body size increased in early amniotes and then increased further in several amniote lineages, notably mammals and birds. The most enlarged regions were the cerebellum and the telencephalon. Within the telencephalon, sauropsids enlarged mainly the ventral pallium, whereas mammals enlarged the dorsal pallium (aka neocortex). Although these regions are not homologous to one another, they both receive unimodal auditory, visual, and somatosensory input from the thalamus.

The Origin of Vertebrates

Some time in the Ediacaran or early Cambrian period, the first vertebrates emerged. Compared to the invertebrate chordates, early vertebrates were active predators, rather than suspension feeders. This change in behavior was facilitated by several major morphological innovations, including pharyngeal muscles that pump water through the pharynx, vascularized gills, paired image-forming eyes, a complex vestibular apparatus, lateral line receptors, taste buds, and a well-developed olfactory system. Early vertebrates also evolved several new brain regions, notably the telencephalon and the midbrain. Developmentally, most of these innovations were linked to the emergence of two novel embryonic tissues, namely placodes and neural crest. Although these tissues and their adult derivatives did not evolve “out of nothing,” they represent genuine innovations that contributed substantially to the evolutionary success of the vertebrate lineage.

The Origin of Jaws and Paired Fins

Between 450 and 500 million years ago, some vertebrates evolved paired fins and jaws, which made them more efficient swimmers and fiercer predators. These jawed vertebrates (i.e., gnathostomes) diversified in the Devonian period, but most died out during the end-Devonian mass extinction. The surviving gnathostomes had a more complex vestibular apparatus than their jawless ancestors, an expanded set of olfactory receptor genes, and vomeronasal receptors. A major innovation in the brains of gnathostomes was the emergence of a cerebellum that is distinct from the cerebellum-like areas found in all vertebrates. The telencephalon of early vertebrates processed primarily olfactory information, but this olfactory dominance was independently reduced in three later lineages, namely in cartilaginous fishes, ray-finned fishes, and tetrapods. In concert with the reduction in olfactory dominance, these lineages enlarged their telencephalon, relative to other brain regions, and evolved a telencephalic “dorsal pallium” that receives non-olfactory sensory information from the diencephalon.

The Rise of Endothermy

Mammals and birds exhibit many examples of convergent evolution, including endothermy and related traits that helped them survive the end-Cretaceous mass extinction. The subsequent diversification of both lineages was accompanied by multiple expansions in relative and (often) absolute brain size. Examples of convergent evolution in the brain include complex folding of the cerebellar cortex, complex auditory circuits, and highly laminar areas within the telencephalon. Of course, birds and mammals also diverged in numerous respects. In particular, early mammals (but not birds!) shifted into a nocturnal niche, which was accompanied by an expansion of the olfactory system and the evolution of highly light-sensitive eyes. In the process, early mammals became “color-blind,” but excellent color vision re-evolved in some diurnal lineages, notably platyrrhine primates. Mammalian brains are also unusual for having strong reciprocal connections between thalamus and dorsal pallium (i.e., neocortex) and extensive commissural connections between the left and right neocortex.

The Invasion of Land

Basal stem tetrapods were fully aquatic but spent time at the water surface breathing air, which was useful at the end of the Devonian, when aquatic oxygen levels were low. After the Devonian, early tetrapods became fully terrestrial, at least as adults. This transition involved major changes in the musculoskeletal system for locomotion and the evolution of new modes of feeding. Aerial vision required changes in the eye but then allowed for high-resolution vision over long distances. In contrast, the lateral line systems are useless in air and were lost in fully terrestrial tetrapods. The brains of early tetrapods were relatively simple, possibly simplified through a process called paedomorphosis. The telencephalon’s main function in early tetrapods was to inhibit or disinhibit the lower brain regions. Later tetrapods diverged into extant amphibians and amniotes. Within the amphibian lineage, anurans evolved a tympanic ear, which increased their ability to hear airborne sounds.

Reconstructing History

This introductory chapter describes the book’s general approach and underlying philosophy. The authors adopt a definition of biological homology that recognizes the hierarchical nature of biological organization and allows for any aspects of a character to change over the course of evolution. The only essential homology criterion is that the characters in question must have been retained from a common ancestor, rather than having evolved independently in multiple lineages. These fundamental ideas are discussed in the context of related concepts, notably “field homology” and the homology of cell types and developmental pathways. Although it is easy to get tangled up in questions about the homology or non-homology of individual characters, the book’s main concern is the evolution and natural history of entire organisms and the lineages to which they belong.