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Two Schools of Evolutionary Thought Evolution of centralized nervous systems: Two schools of evolutionary thought R. Glenn Northcutt1 Laboratory of Comparative Neurobiology, Scripps Institution of Oceanography and Department of Neurosciences, University of California at San Diego, La Jolla, CA 92093 Edited by John C. Avise, University of California, Irvine, CA, and approved May 1, 2012 (received for review February 27, 2012) Understanding the evolution of centralized nervous systems Fossil Record requires an understanding of metazoan phylogenetic interrela- The fossil record is notoriously incomplete. Fossils essentially exist tionships, their fossil record, the variation in their cephalic neural as snapshots in time, and these snapshots are of varying quality. characters, and the development of these characters. Each of these Some are grainy, providing only a glimpse of organisms and their topics involves comparative approaches, and both cladistic and ecology; others are fine-grained photographs of individual taxa phenetic methodologies have been applied. Our understanding of and their ecology (Lagerstätten). Regardless, each snapshot metazoan phylogeny has increased greatly with the cladistic provides unique and critical insights into the minimal age of a analysis of molecular data, and relaxed molecular clocks gener- radiation. Each snapshot helps calibrate molecular clocks, establish ally date the origin of bilaterians at 600–700 Mya (during the ecological settings of evolutionary events, and reveal unsuspected Ediacaran). Although the taxonomic affinities of the Ediacaran bi- morphological characters that challenge current conclusions re- ota remain uncertain, a conservative interpretation suggests that garding character transformation (2). a number of these taxa form clades that are closely related, if not stem clades of bilaterian crown clades. Analysis of brain–body Ediacaran Biota. The earliest reported fossils of possible metazoan complexity among extant bilaterians indicates that diffuse nerve embryos and adults are in the Ediacaran Doushantuo Formation nets and possibly, ganglionated cephalic neural systems existed in (∼570 Mya) in southern China (3–5). Small globular fossils, ∼200 Ediacaran organisms. An outgroup analysis of cephalic neural char- μm in diameter, show remarkable cellular details and have been acters among extant metazoans also indicates that the last com- interpreted as cnidarian gastrulae and planulae as well as bilaterian mon bilaterian ancestor possessed a diffuse nerve plexus and that gastrulae comparable with living molluscans and echinoderms (4). brains evolved independently at least four times. In contrast, the However, the interpretation of these fossils as bilaterian meta- hypothesis of a tripartite brain, based primarily on phenetic analysis zoans has been questioned, and they have been reinterpreted as of developmental genetic data, indicates that the brain arose in the encysted holozoan protists (6). Similar problems plague the last common bilaterian ancestor. Hopefully, this debate will be re- earliest reported adult bilaterian, Vernanimalcula,whichisalso solved by cladistic analysis of the genomes of additional taxa and an from the Doushantuo Formation of southern China (7, 8). Fossils increased understanding of character identity genetic networks. of Vernanimalcula (∼200 μm in diameter) have been described as broadly oval and triploblastic with a mouth, a differentiated gut Cambrian explosion | Neoproterozoic | phyletic comparisons | Urbilateria surrounded by paired coeloms, and an anus. The rostral end of these “small spring animals” is also reported to have three pairs of external pits that have been interpreted as sensory organs (7). The fact that some of these building stones are universal does not, of This interpretation has been questioned, however, and these course, mean that the organs to which they contribute are as old as fossils have been claimed to be taphonomic artifacts in which these molecules or their precursors. phosphates were deposited within a spherical object, such as the cysts of algal acritarchs (9). von Salvini-Plawen and Mayr (1) The earliest fossils of macroscopic organisms interpreted as ny consideration of the evolution of centralized nervous metazoans, including bilaterians, are in the Ediacaran strata Asystems is inextricably linked to an understanding of the above the Doushantuo formation (10). They average 10 cm but phylogeny of living metazoans, their fossil history, the vast range reach an extreme of 1 m in length, and they include forms that A of complexity in their nervous systems, and the development of are frond-, disk-, and worm-like (Fig. 1 ); their interpretation has had a tumultuous history. Many of these fossils were discovered in these nervous systems. For this reason, any attempt to reconstruct the late 1940s and were interpreted as representatives of living the phylogeny of metazoan CNSs must be based on all lines of metazoan phyla. Forms like Eoporpita (Fig. 1A, 1) were inter- evidence available. The molecular phylogenetic studies of the preted as cnidarian pelagic medusa (11), and frond-like forms, last 20 y are particularly important in understanding metazoan such as Charniodiscus (Fig. 1A, 2), were interpreted as possible interrelationships as well as the time frame in which these animals cnidarian sea pins (12). Still other forms of these fossils were arose and radiated, and we now have increased insights into the interpreted as stem bilaterians. For example, Dickinsonia (Fig. 1A, genetics underlying the development of CNSs. 3) was interpreted as a flatworm (13), Arkarua (Fig. 1A, 4) was First, I will review the fossil history of the earliest putative met- interpreted as an echinoderm (14), Spriggina (Fig. 1A, 5) was azoans, and then, I will discuss different comparative approaches to analyzing both molecular and morphological data: the mo- lecular clock hypothesis, which has yielded a range of possible This paper results from the Arthur M. Sackler Colloquium of the National Academy of dates for the origin and divergence of metazoans; developmental Sciences, “In the Light of Evolution VI: Brain and Behavior,” held January 19–21, 2012, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engi- genetics and its contribution to our understanding of the pat- neering in Irvine, CA. The complete program and audio files of most presentations are terning of metazoan bodies, particularly patterning of the CNS; available on the NAS Web site at www.nasonline.org/evolution_vi. and conclusions based on the first outgroup analysis of metazoan Author contributions: R.G.N. analyzed data and wrote the paper. central neural characters. Finally, I will review two hypotheses The author declares no conflict of interest. concerning the morphological complexity of the last common This article is a PNAS Direct Submission. bilaterian ancestor. 1E-mail: [email protected]. 10626–10633 | PNAS | June 26, 2012 | vol. 109 | suppl. 1 www.pnas.org/cgi/doi/10.1073/pnas.1201889109 Downloaded by guest on September 27, 2021 Fig. 1. Reconstruction of the Ediacaran (A) and Burgess Shale (B) biotas. The Ediacaran biota is reconstructed to convey maximal morphological complexity. (A)1,Eoporpita;2,Charniodiscus;3,Dickinsonia;4,Arkarua;5,Spriggina;6,Praecambridium; 7, soft-bodied “trilobite”;8,Kimberella.(B)1,Burgessochaeta; 2, Lingulella;3,Ottoia;4,Marrella;5,Olenoides;6,Naraoia;7,Canadaspis;8,Sidneyia,9,Opabinia;10,Anomalocaris; 11, Gogia;12,Eldonia; 13, Pikaia;14, Aysheaia; 15, Hallucigenia; 16, Odontogriphus; 17, Dinomischus. interpreted as an annelid capable of active swimming (15), and the White Sea assemblage are diverse and suggest the presence Praecambridium (Fig. 1A, 6) and a soft-bodied “trilobite” not for- of small bilaterians (21). mally described (Fig. 1A, 7) were interpreted as stem arthropods The Nama assemblage has less diversity than either the Avalon (16, 17). After this burst of descriptions, Ediacaran anatomy was or White Sea assemblages, and it is dominated by frond-like taxa, reevaluated; claims were made that all Ediacarans were orga- called arboreomorphs, and simple cylindrical, sessile taxa, called nized on a quilt-like pattern and represented an independent erniettomorphs (21, 22). Bilaterian body fossils are absent, but experiment of nonmetazoan animals, termed the Vendobionta, small calcified shells of Cloudina and Namacalathus and the ear- that failed with the evolution of macrophagous bilaterian meta- liest evidence of predation in the form of holes bored into these zoans (18–20). The concept of the Ediacaran biota as Vendobionta calcified shells do occur (26). was generally abandoned, because paleontologists came to realize Our understanding of body organization and phylogeny of that the Ediacaran biota represents a wide range of morphological Ediacarans is incomplete, but a conservative interpretation of forms (10, 21). the paleontological data indicates that most animals existed To date, the Ediacaran biota includes some 160 taxa (10) found primarily on microbial mats; it was likely a 2D world, with sessile in 40 separate locations representing all parts of the globe except frond-like forms and vagile, small organisms that trophically Antarctica. These biotas are dispersed among three stratigraphic were suspension feeders and grazers. There is little to no evidence zones in named assemblages based on a cladistic analysis of their that pelagic medusae existed (Fig. 1A, 1), but there is considerable spatial and temporal distribution (22): an Avalon
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