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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Feb 28;353(1366):327–345. doi: 10.1098/rstb.1998.0213

The evolution of diversity in ancient ecosystems: a review

S Conway Morris
PMCID: PMC1692204

Abstract

On a perfect planet, such as might be acceptable to a physicist, one might predict that from its origin the diversity of life would grow exponentially until the carrying capacity, however defined, was reached. The fossil record of the Earth, however, tells a very different story. One of the most striking aspects of this record is the apparent evolutionary longueur, marked by the Precambrian record of prokaryotes and primitive eukaryotes, although our estimates of microbial diversity may be seriously incomplete. Subsequently there were various dramatic increases in diversity, including the Cambrian 'explosion' and the radiation of Palaeozoic-style faunas in the Ordovician. The causes of these events are far from resolved. It has also long been appreciated that the history of diversity has been punctuated by important extinctions. The subtleties and nuances of extinction as well as the survival of particular clades have to date, however, received rather too little attention, and there is still a tendency towards blanket assertions rather than a dissection of these extraordinary events. In addition, some but perhaps not all mass extinctions are characterized by long lag-times of recovery, which may reflect the slowing waning of extrinsic forcing factors or alternatively the incoherence associated with biological reassembly of stable ecosystems. The intervening periods between the identified mass extinctions may be less stable and benign than popularly thought, and in particular the frequency of extraterrestrial impacts leads to predictions of recurrent disturbance on timescales significantly shorter than the intervals separating the largest extinction events. Even at times of quietude it is far from clear whether biological communities enjoy stability and interlocked stasis or are dynamically reconstituted at regular intervals. Finally, can we yet rely on the present depictions of the rise and falls in the levels of ancient diversity? Existing data is almost entirely based on Linnean taxa, and the application of phylogenetic systematics to this problem is still in its infancy. Not only that, but even more intriguingly the pronounced divergence in estimates of origination times of groups as diverse as angiosperms, diatoms and mammals in terms of the fossil record as against molecular data point to the possibilities of protracted intervals of geological time with a cryptic diversity. If this is correct, and there are alternative explanations, then some of the mystery of adaptive radiations may be dispelled, in as much as the assembly of key features in the stem groups could be placed in a gradualistic framework of local adaptive response punctuated by intervals of opportunity.

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Selected References

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  1. Alvarez W., Claeys P., Kieffer S. W. Emplacement of cretaceous-tertiary boundary shocked quartz from chicxulub crater. Science. 1995 Aug 18;269(5226):930–935. doi: 10.1126/science.269.5226.930. [DOI] [PubMed] [Google Scholar]
  2. Archibald JD. Fossil Evidence for a Late Cretaceous Origin of "Hoofed" Mammals. Science. 1996 May 24;272(5265):1150–1153. doi: 10.1126/science.272.5265.1150. [DOI] [PubMed] [Google Scholar]
  3. Awramik S. M. Precambrian columnar stromatolite diversity: reflection of metazoan appearance. Science. 1971 Nov 19;174(4011):825–827. doi: 10.1126/science.174.4011.825. [DOI] [PubMed] [Google Scholar]
  4. Barns S. M., Delwiche C. F., Palmer J. D., Dawson S. C., Hershberger K. L., Pace N. R. Phylogenetic perspective on microbial life in hydrothermal ecosystems, past and present. Ciba Found Symp. 1996;202:24–39. doi: 10.1002/9780470514986.ch2. [DOI] [PubMed] [Google Scholar]
  5. Barns S. M., Delwiche C. F., Palmer J. D., Pace N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9188–9193. doi: 10.1073/pnas.93.17.9188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benton M. J. Diversification and extinction in the history of life. Science. 1995 Apr 7;268(5207):52–58. doi: 10.1126/science.7701342. [DOI] [PubMed] [Google Scholar]
  7. Bice D. M., Newton C. R., McCauley S., Reiners P. W., McRoberts C. A. Shocked quartz at the triassic-jurassic boundary in Italy. Science. 1992 Jan 24;255(5043):443–446. doi: 10.1126/science.255.5043.443. [DOI] [PubMed] [Google Scholar]
  8. Buzas M. A., Culver S. J. Species pool and dynamics of marine paleocommunities. Science. 1994 Jun 3;264(5164):1439–1441. doi: 10.1126/science.264.5164.1439. [DOI] [PubMed] [Google Scholar]
  9. Clark D. L., Cheng-Yuan W., Orth C. J., Gilmore J. S. Conodont survival and low iridium abundances across the permian-triassic boundary in South china. Science. 1986 Aug 29;233(4767):984–986. doi: 10.1126/science.233.4767.984. [DOI] [PubMed] [Google Scholar]
  10. Cronin T. M. Speciation and stasis in marine ostracoda: climatic modulation of evolution. Science. 1985 Jan 4;227(4682):60–63. doi: 10.1126/science.227.4682.60. [DOI] [PubMed] [Google Scholar]
  11. Doolittle R. F., Feng D. F., Tsang S., Cho G., Little E. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science. 1996 Jan 26;271(5248):470–477. doi: 10.1126/science.271.5248.470. [DOI] [PubMed] [Google Scholar]
  12. Foote M., Raup D. M. Fossil preservation and the stratigraphic ranges of taxa. Paleobiology. 1996 Spring;22(2):121–140. doi: 10.1017/s0094837300016134. [DOI] [PubMed] [Google Scholar]
  13. Frye M. S., Hedges S. B. Monophyly of the order Rodentia inferred from mitochondrial DNA sequences of the genes for 12S rRNA, 16S rRNA, and tRNA-valine. Mol Biol Evol. 1995 Jan;12(1):168–176. doi: 10.1093/oxfordjournals.molbev.a040186. [DOI] [PubMed] [Google Scholar]
  14. Garrett P. Phanerozoic stromatolites: noncompetitive ecologic restriction by grazing and burrowing animals. Science. 1970 Jul 10;169(3941):171–173. doi: 10.1126/science.169.3941.171. [DOI] [PubMed] [Google Scholar]
  15. Grotzinger J. P., Knoll A. H. Anomalous carbonate precipitates: is the Precambrian the key to the Permian? Palaios. 1995 Dec;10(6):578–596. [PubMed] [Google Scholar]
  16. Han T. M., Runnegar B. Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. Science. 1992 Jul 10;257(5067):232–235. doi: 10.1126/science.1631544. [DOI] [PubMed] [Google Scholar]
  17. Hedges S. B., Parker P. H., Sibley C. G., Kumar S. Continental breakup and the ordinal diversification of birds and mammals. Nature. 1996 May 16;381(6579):226–229. doi: 10.1038/381226a0. [DOI] [PubMed] [Google Scholar]
  18. Hunter J. P., Jernvall J. The hypocone as a key innovation in mammalian evolution. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10718–10722. doi: 10.1073/pnas.92.23.10718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Härlid A., Janke A., Arnason U. The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. Mol Biol Evol. 1997 Jul;14(7):754–761. doi: 10.1093/oxfordjournals.molbev.a025815. [DOI] [PubMed] [Google Scholar]
  20. Jablonski D., Sepkoski J. J., Jr Paleobiology, community ecology, and scales of ecological pattern. Ecology. 1996 Jul;77(5):1367–1378. [PubMed] [Google Scholar]
  21. Jablonski D. The biology of mass extinction: a palaeontological view. Philos Trans R Soc Lond B Biol Sci. 1989;325:357–368. doi: 10.1098/rstb.1989.0093. [DOI] [PubMed] [Google Scholar]
  22. Janke A., Feldmaier-Fuchs G., Thomas W. K., von Haeseler A., Päbo S. The marsupial mitochondrial genome and the evolution of placental mammals. Genetics. 1994 May;137(1):243–256. doi: 10.1093/genetics/137.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Knoll A. H., Bambach R. K., Canfield D. E., Grotzinger J. P. Comparative Earth history and Late Permian mass extinction. Science. 1996 Jul 26;273:452–457. [PubMed] [Google Scholar]
  24. Knoll A. H. Proterozoic and early Cambrian protists: evidence for accelerating evolutionary tempo. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6743–6750. doi: 10.1073/pnas.91.15.6743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Knoll A. H., Walter M. R. The limits of palaeontological knowledge: finding the gold among the dross. Ciba Found Symp. 1996;202:198–213. doi: 10.1002/9780470514986.ch11. [DOI] [PubMed] [Google Scholar]
  26. Kolukisaoglu H. U., Marx S., Wiegmann C., Hanelt S., Schneider-Poetsch H. A. Divergence of the phytochrome gene family predates angiosperm evolution and suggests that Selaginella and Equisetum arose prior to Psilotum. J Mol Evol. 1995 Sep;41(3):329–337. [PubMed] [Google Scholar]
  27. Labandeira C. C., Sepkoski J. J., Jr Insect diversity in the fossil record. Science. 1993 Jul 16;261(5119):310–315. doi: 10.1126/science.11536548. [DOI] [PubMed] [Google Scholar]
  28. Levinton J. S., Ginzburg L. Repeatability of taxon longevity in successive foraminifera radiations and a theory of random appearance and extinction. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5478–5481. doi: 10.1073/pnas.81.17.5478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Logan G. A., Hayes J. M., Hieshima G. B., Summons R. E. Terminal Proterozoic reorganization of biogeochemical cycles. Nature. 1995 Jul 6;376(6535):53–56. doi: 10.1038/376053a0. [DOI] [PubMed] [Google Scholar]
  30. Martin W., Lydiate D., Brinkmann H., Forkmann G., Saedler H., Cerff R. Molecular phylogenies in angiosperm evolution. Mol Biol Evol. 1993 Jan;10(1):140–162. doi: 10.1093/oxfordjournals.molbev.a039989. [DOI] [PubMed] [Google Scholar]
  31. Miller A. I., Foote M. Calibrating the Ordovician Radiation of marine life: implications for Phanerozoic diversity trends. Paleobiology. 1996 Spring;22(2):304–309. doi: 10.1666/0094-8373-22.2.304. [DOI] [PubMed] [Google Scholar]
  32. Morris S. C. Defusing the Cambrian 'explosion'? Curr Biol. 1997 Feb 1;7(2):R71–R74. doi: 10.1016/s0960-9822(06)00039-x. [DOI] [PubMed] [Google Scholar]
  33. Odorico D. M., Miller D. J. Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol Biol Evol. 1997 May;14(5):465–473. doi: 10.1093/oxfordjournals.molbev.a025783. [DOI] [PubMed] [Google Scholar]
  34. Orth C. J., Knight J. D., Quintana L. R., Gilmore J. S., Palmer A. R. A search for iridium abundance anomalies at two late cambrian biomere boundaries in Western utah. Science. 1984 Jan 13;223(4632):163–165. doi: 10.1126/science.223.4632.163. [DOI] [PubMed] [Google Scholar]
  35. doi: 10.1098/rspb.1997.0057. [DOI] [PMC free article] [Google Scholar]
  36. Pawlowski J., Bolivar I., Fahrni J. F., Cavalier-Smith T., Gouy M. Early origin of foraminifera suggested by SSU rRNA gene sequences. Mol Biol Evol. 1996 Mar;13(3):445–450. doi: 10.1093/oxfordjournals.molbev.a025605. [DOI] [PubMed] [Google Scholar]
  37. Pawlowski J., Bolivar I., Fahrni J. F., de Vargas C., Gouy M., Zaninetti L. Extreme differences in rates of molecular evolution of foraminifera revealed by comparison of ribosomal DNA sequences and the fossil record. Mol Biol Evol. 1997 May;14(5):498–505. doi: 10.1093/oxfordjournals.molbev.a025786. [DOI] [PubMed] [Google Scholar]
  38. Pawlowski J., Bolivar I., Guiard-Maffia J., Gouy M. Phylogenetic position of foraminifera inferred from LSU rRNA gene sequences. Mol Biol Evol. 1994 Nov;11(6):929–938. doi: 10.1093/oxfordjournals.molbev.a040174. [DOI] [PubMed] [Google Scholar]
  39. Pope K. O., Baines K. H., Ocampo A. C., Ivanov B. A. Impact winter and the Cretaceous/Tertiary extinctions: results of a Chicxulub asteroid impact model. Earth Planet Sci Lett. 1994;128:719–725. doi: 10.1016/0012-821x(94)90186-4. [DOI] [PubMed] [Google Scholar]
  40. Raup D. M., Jablonski D. Geography of end-Cretaceous marine bivalve extinctions. Science. 1993 May 14;260:971–973. doi: 10.1126/science.11537491. [DOI] [PubMed] [Google Scholar]
  41. Raup D. M. Large-body impact and extinction in the Phanerozoic. Paleobiology. 1992 Winter;18(1):80–88. doi: 10.1017/s0094837300012227. [DOI] [PubMed] [Google Scholar]
  42. Raup D. M., Sepkoski J. J., Jr Periodic extinction of families and genera. Science. 1986 Feb 21;231:833–836. doi: 10.1126/science.11542060. [DOI] [PubMed] [Google Scholar]
  43. Raup D. M. Size of the permo-triassic bottleneck and its evolutionary implications. Science. 1979 Oct 12;206(4415):217–218. doi: 10.1126/science.206.4415.217. [DOI] [PubMed] [Google Scholar]
  44. Runnegar B. Collagen gene construction and evolution. J Mol Evol. 1985;22(2):141–149. doi: 10.1007/BF02101692. [DOI] [PubMed] [Google Scholar]
  45. Schluter D. Experimental evidence that competition promotes divergence in adaptive radiation. Science. 1994 Nov 4;266(5186):798–801. doi: 10.1126/science.266.5186.798. [DOI] [PubMed] [Google Scholar]
  46. Sepkoski J. J., Jr A model of onshore-offshore change in faunal diversity. Paleobiology. 1991;17(1):58–77. doi: 10.1017/s0094837300010356. [DOI] [PubMed] [Google Scholar]
  47. Sepkoski J. J., Jr Alpha, beta, or gamma: where does all the diversity go? Paleobiology. 1988;14(3):221–234. doi: 10.1017/s0094837300011969. [DOI] [PubMed] [Google Scholar]
  48. Sepkoski J. J., Jr Biodiversity: past, present, and future. J Paleontol. 1997 Jul;71(4):533–539. doi: 10.1017/s0022336000040026. [DOI] [PubMed] [Google Scholar]
  49. Sepkoski J. J., Jr, Kendrick D. C. Numerical experiments with model monophyletic and paraphyletic taxa. Paleobiology. 1993;19(2):168–184. doi: 10.1017/s0094837300015852. [DOI] [PubMed] [Google Scholar]
  50. Sepkoski J. J., Jr Ten years in the library: new data confirm paleontological patterns. Paleobiology. 1993 Winter;19(1):43–51. doi: 10.1017/s0094837300012306. [DOI] [PubMed] [Google Scholar]
  51. Solé R. V., Bascompte J. Are critical phenomena relevant to large-scale evolution? Proc Biol Sci. 1996 Feb 22;263(1367):161–168. doi: 10.1098/rspb.1996.0026. [DOI] [PubMed] [Google Scholar]
  52. Spring J. Vertebrate evolution by interspecific hybridisation--are we polyploid? FEBS Lett. 1997 Jan 2;400(1):2–8. doi: 10.1016/s0014-5793(96)01351-8. [DOI] [PubMed] [Google Scholar]
  53. Springer M. S., Cleven G. C., Madsen O., de Jong W. W., Waddell V. G., Amrine H. M., Stanhope M. J. Endemic African mammals shake the phylogenetic tree. Nature. 1997 Jul 3;388(6637):61–64. doi: 10.1038/40386. [DOI] [PubMed] [Google Scholar]
  54. Summons R. E., Jahnke L. L., Simoneit B. R. Lipid biomarkers for bacterial ecosystems: studies of cultured organisms, hydrothermal environments and ancient sediments. Ciba Found Symp. 1996;202:174–194. doi: 10.1002/9780470514986.ch10. [DOI] [PubMed] [Google Scholar]
  55. Surlyk F., Johansen M. B. End-cretaceous brachiopod extinctions in the chalk of denmark. Science. 1984 Mar 16;223(4641):1174–1177. doi: 10.1126/science.223.4641.1174. [DOI] [PubMed] [Google Scholar]
  56. Sussman G. J., Wisdom J. Chaotic evolution of the solar system. Science. 1992 Jul 3;257(5066):56–62. doi: 10.1126/science.257.5066.56. [DOI] [PubMed] [Google Scholar]
  57. Syvanen M. Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet. 1994;28:237–261. doi: 10.1146/annurev.ge.28.120194.001321. [DOI] [PubMed] [Google Scholar]
  58. Teig E., Lindeman H. H., Tvete O., Hanche-Olsen S., Rasmussen K. Audiovisual test programs in native languages. Test material in Norwegian on a video disc controlled by laser bar code. Adv Otorhinolaryngol. 1993;48:199–202. [PubMed] [Google Scholar]
  59. Valentine J. W., Erwin D. H., Jablonski D. Developmental evolution of metazoan bodyplans: the fossil evidence. Dev Biol. 1996 Feb 1;173(2):373–381. doi: 10.1006/dbio.1996.0033. [DOI] [PubMed] [Google Scholar]
  60. Valentine J. W. Phanerozoic taxonomic diversity: a test of alternate models. Science. 1973 Jun 8;180(4090):1078–1079. doi: 10.1126/science.180.4090.1078. [DOI] [PubMed] [Google Scholar]
  61. Wade C. M., Darling K. F., Kroon D., Leigh Brown A. J. Early evolutionary origin of the planktic foraminifera inferred from small subunit rDNA sequence comparisons. J Mol Evol. 1996 Dec;43(6):672–677. doi: 10.1007/BF02202115. [DOI] [PubMed] [Google Scholar]
  62. Walter M. R. Ancient hydrothermal ecosystems on earth: a new palaeobiological frontier. Ciba Found Symp. 1996;202:112–130. doi: 10.1002/9780470514986.ch7. [DOI] [PubMed] [Google Scholar]
  63. Wolfe K. H., Gouy M., Yang Y. W., Sharp P. M., Li W. H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6201–6205. doi: 10.1073/pnas.86.16.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]

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