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The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution.
Biol Rev Camb Philos Soc. 2017 Feb; 92(1):446-473.BR

Abstract

The earliest evolution of the animals remains a taxing biological problem, as all extant clades are highly derived and the fossil record is not usually considered to be helpful. The rise of the bilaterian animals recorded in the fossil record, commonly known as the 'Cambrian explosion', is one of the most significant moments in evolutionary history, and was an event that transformed first marine and then terrestrial environments. We review the phylogeny of early animals and other opisthokonts, and the affinities of the earliest large complex fossils, the so-called 'Ediacaran' taxa. We conclude, based on a variety of lines of evidence, that their affinities most likely lie in various stem groups to large metazoan groupings; a new grouping, the Apoikozoa, is erected to encompass Metazoa and Choanoflagellata. The earliest reasonable fossil evidence for total-group bilaterians comes from undisputed complex trace fossils that are younger than about 560 Ma, and these diversify greatly as the Ediacaran-Cambrian boundary is crossed a few million years later. It is generally considered that as the bilaterians diversified after this time, their burrowing behaviour destroyed the cyanobacterial mat-dominated substrates that the enigmatic Ediacaran taxa were associated with, the so-called 'Cambrian substrate revolution', leading to the loss of almost all Ediacara-aspect diversity in the Cambrian. Why, though, did the energetically expensive and functionally complex burrowing mode of life so typical of later bilaterians arise? Here we propose a much more positive relationship between late-Ediacaran ecologies and the rise of the bilaterians, with the largely static Ediacaran taxa acting as points of concentration of organic matter both above and below the sediment surface. The breaking of the uniformity of organic carbon availability would have signalled a decisive shift away from the essentially static and monotonous earlier Ediacaran world into the dynamic and burrowing world of the Cambrian. The Ediacaran biota thus played an enabling role in bilaterian evolution similar to that proposed for the Savannah environment for human evolution and bipedality. Rather than being obliterated by the rise of the bilaterians, the subtle remnants of Ediacara-style taxa within the Cambrian suggest that they remained significant components of Phanerozoic communities, even though at some point their enabling role for bilaterian evolution was presumably taken over by bilaterians or other metazoans. Bilaterian evolution was thus an essentially benthic event that only later impacted the planktonic environment and the style of organic export to the sea floor.

Authors+Show Affiliations

Palaeobiology Programme, Department of Earth Sciences, Uppsala University, Villavägen 16, SE 752 40, Uppsala, Sweden.Área de Paleontología, Facultad de Ciencias, Universidad de Extremadura, 06006, Badajoz, Spain.

Pub Type(s)

Journal Article
Review

Language

eng

PubMed ID

26588818

Citation

Budd, Graham E., and Sören Jensen. "The Origin of the Animals and a 'Savannah' Hypothesis for Early Bilaterian Evolution." Biological Reviews of the Cambridge Philosophical Society, vol. 92, no. 1, 2017, pp. 446-473.
Budd GE, Jensen S. The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution. Biol Rev Camb Philos Soc. 2017;92(1):446-473.
Budd, G. E., & Jensen, S. (2017). The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution. Biological Reviews of the Cambridge Philosophical Society, 92(1), 446-473. https://doi.org/10.1111/brv.12239
Budd GE, Jensen S. The Origin of the Animals and a 'Savannah' Hypothesis for Early Bilaterian Evolution. Biol Rev Camb Philos Soc. 2017;92(1):446-473. PubMed PMID: 26588818.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution. AU - Budd,Graham E, AU - Jensen,Sören, Y1 - 2015/11/20/ PY - 2015/02/25/received PY - 2015/10/12/revised PY - 2015/10/21/accepted PY - 2015/11/21/pubmed PY - 2018/1/31/medline PY - 2015/11/21/entrez KW - Apoikozoa KW - Cambrian explosion KW - Kimberella KW - animal origins KW - ecology KW - ediacarans KW - evolution KW - heterogeneity KW - stem groups KW - trace fossils SP - 446 EP - 473 JF - Biological reviews of the Cambridge Philosophical Society JO - Biol Rev Camb Philos Soc VL - 92 IS - 1 N2 - The earliest evolution of the animals remains a taxing biological problem, as all extant clades are highly derived and the fossil record is not usually considered to be helpful. The rise of the bilaterian animals recorded in the fossil record, commonly known as the 'Cambrian explosion', is one of the most significant moments in evolutionary history, and was an event that transformed first marine and then terrestrial environments. We review the phylogeny of early animals and other opisthokonts, and the affinities of the earliest large complex fossils, the so-called 'Ediacaran' taxa. We conclude, based on a variety of lines of evidence, that their affinities most likely lie in various stem groups to large metazoan groupings; a new grouping, the Apoikozoa, is erected to encompass Metazoa and Choanoflagellata. The earliest reasonable fossil evidence for total-group bilaterians comes from undisputed complex trace fossils that are younger than about 560 Ma, and these diversify greatly as the Ediacaran-Cambrian boundary is crossed a few million years later. It is generally considered that as the bilaterians diversified after this time, their burrowing behaviour destroyed the cyanobacterial mat-dominated substrates that the enigmatic Ediacaran taxa were associated with, the so-called 'Cambrian substrate revolution', leading to the loss of almost all Ediacara-aspect diversity in the Cambrian. Why, though, did the energetically expensive and functionally complex burrowing mode of life so typical of later bilaterians arise? Here we propose a much more positive relationship between late-Ediacaran ecologies and the rise of the bilaterians, with the largely static Ediacaran taxa acting as points of concentration of organic matter both above and below the sediment surface. The breaking of the uniformity of organic carbon availability would have signalled a decisive shift away from the essentially static and monotonous earlier Ediacaran world into the dynamic and burrowing world of the Cambrian. The Ediacaran biota thus played an enabling role in bilaterian evolution similar to that proposed for the Savannah environment for human evolution and bipedality. Rather than being obliterated by the rise of the bilaterians, the subtle remnants of Ediacara-style taxa within the Cambrian suggest that they remained significant components of Phanerozoic communities, even though at some point their enabling role for bilaterian evolution was presumably taken over by bilaterians or other metazoans. Bilaterian evolution was thus an essentially benthic event that only later impacted the planktonic environment and the style of organic export to the sea floor. SN - 1469-185X UR - https://www.unboundmedicine.com/medline/citation/26588818/The_origin_of_the_animals_and_a_'Savannah'_hypothesis_for_early_bilaterian_evolution_ L2 - https://doi.org/10.1111/brv.12239 DB - PRIME DP - Unbound Medicine ER -