- Email: [email protected]
Reply from A.L.R. Thomas
CORRESPONDENCE Cambrian explosion still in the water
Reply from A.L.R. Thomas
Was Adrian Thomas’s short note in the last issue of TREE 1 intended to be provocative? The Cambrian explosion has not been ‘blown out of the water’. First, the existence of late Precambrian metazoan fossils does not alter the fact that Cambrian fossils record an explosive diversification of animals, although it may make it easier to explain. Second, it has been many years since the fossil record of metazoan animals started with the Cambrian explosion – I first learned about the late Precambrian Ediacara fauna when I was an undergraduate 25 years ago and it was not particularly new to science then. The recent discovery of fossilized metazoan embryos in 570 million-year-old Precambrian rocks in China2 is tremendously exciting, but it is not the first indication of a metazoan fossil record predating the Cambrian explosion. The Ediacara fauna (now known as Vendozoa or Vendobionta), once shoehorned into extant phyla, has been interpreted as representing an early radiation of metazoans3 that were not closely related to Cambrian metazoan animals and that flourished during the last 60 million years (very approximately) of the Precambrian but became extinct before the Cambrian explosion. The Chinese fossil embryos may represent the oldest fossils of metazoans that were directly ancestral to Phanerozoic (Cambrian onwards) lineages. A plausible explanation has been put forward (also reported in the same issue of TREE ) that the vendozoans occupied the ecological niches available to large animals (several cm), restricting Precambrian (late Proterozoic and Vendian) precursors of Phanerozoic metazoans to small size (mm) and, therefore, little chance of fossilization4. The Cambrian explosion can then be attributed partly to a size increase of ‘Phanerozoic Metazoa’ once the vendozoans became extinct. In terms of the fossil record of all metazoans, the vendozoans could even predate the latest Chinese findings. Recent dating of the Ediacara fauna of the English Midlands suggests that it has a minimum age of 603 ± 2 million years, although the authors5 are cautious about the accuracy of this figure. The fossil record has enough gaps in it – let’s not introduce more through forgetfulness!
Horne chides me for enhancing the gaps in the fossil record through ‘forgetfulness’ and for being provocative in ignoring the Precambrian Ediacara fauna. Space constraints aside, I claim two mitigating circumstances: First, both Bell1 and I reviewed the substantial evidence in favour of a long Precambrian history of the metazoans (e.g. widespread trace fossils and possible fossilized metazoan faecal pellets, and decline in stromatolite diversity and abundance from about 1000 million years ago onwards), and the most likely reason why they did not fossilize easily before the Cambrian (because atmospheric oxygen levels fell below a critical threshold for the formation of hard body parts) in TREE last year2. Second, the Ediacaran fauna are so enigmatic as to be uninformative. The Ediacaran fauna have been described as lichens3 or as an entirely separate experiment in multicellularity4, but recent analyses suggest that they might be nothing more exciting than fossils of conventional metazoans5,6. The argument over these fossils may be intense precisely because they are enigmatic. The Ediacaran sites I have visited in Sweden are striking for their beautiful preservation of the Precambrian sea floor, and for the astonishing abundance of trace fossils they contain, but the Ediacaran fossils (mostly Psammocoralia) are most impressive for their lack of discernible features. On the charge of being provocative, I claim no credit for that – the discovery of these fossils is in itself both exciting and provocative. These Precambrian metazoan embryo fossils at last provide a clear refutation of the idea that the Cambrian explosion represents the sudden emergence of all the metazoan phyla in a few short millions of years, and there is no longer any need to resort to anything other than conventional, gradual, progressive darwinian evolution to account for the origins of the metazoa. The Cambrian explosion is now clearly identified as a taphonomic event, marking the evolution (in only about two-thirds of the metazoan phyla) of features permitting fossilization. As Darwin7 predicted, and as a series of recent molecular analyses have confirmed8, the metazoa underwent a period of cryptic evolution before the Cambrian that was as long or longer than has elapsed since.
David J. Horne
A.L.R. Thomas
School of Earth & Environmental Sciences, University of Greenwich, Chatham Maritime, Kent, UK ME4 4TB ([email protected])
Dept of Zoology, University of Oxford, South Parks Road, Oxford, UK OX1 3PS ([email protected]) References
References 1 Thomas, A.L.R. (1998) Trends Ecol. Evol. 13, 129 2 Xiao, S., Zhang, Y. and Knoll, A.H. (1998) Nature 391, 553 –558 3 Seilacher, A. (1989) Lethaia 22, 229–239 4 Cooper, A. and Fortey, R. (1998) Trends Ecol. Evol. 13, 151–156 5 McIlroy, D., Brasier, M.D. and Moseley, J.B. (1998) J. Geol. Soc. Lond. 155, 401– 411
322
1 Bell, M.A. (1997) Trends Ecol. Evol. 12, 1–2 2 Thomas, A.L.R. (1997) Trends Ecol. Evol. 128, 44 – 45 3 Retallack, G.J. (1994) Paleobiology 20, 523 –544 4 Buss, L.W. and Seilacher, A. (1994) Paleobiology 20, 1– 4 5 Conway Morris, S. (1993) Nature 361, 219 –225 6 Fedonkin, M.A. and Waggoner, B.M. (1997) Nature 388, 868 – 871
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00
7 Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, Murray 8 Li, C-W., Chen, J-Y. and Hua, T-E. (1998) Science 279, 879 – 882
Female song for mate attraction: an overlooked phenomenon? In her recent TREE review, Langmore looked in detail at possible functions of female song in birds1. Although it is now generally accepted that males sing to attract females2,3, Langmore concludes that the attraction of mates does not appear to be a common function of female song. Here, we would like to draw attention to several observations that suggest that a mate attraction function of song might be more common in females than previously thought. First, Drent observed that female great tits (Parus major ), start singing after losing their mate, irrespective of whether they are inside or outside the territory of their former mate (P.J. Drent, PhD thesis, University of Groningen, 1983). He further observed that once females had obtained a mate again, spontaneous song declined almost completely. These observations suggest that female great tits use song to attract a new male. Second, in another tit species, the blue tit (Parus caeruleus ), Kempenaers and co-workers4 removed nine males for about one hour during the fertile period of their female, and they observed that all females started giving contact calls immediately and two of them also started singing, lending further support to the idea that females use song to attract their own or a new male. Third, Snow 5 also described that a female blackbird (Turdus merula ), started singing after having lost her male. Fourth, female canaries (Serinus canaria ), have been reported to sing frequently if they are kept isolated from males 6,7. Finally, knowing that male song is important in the context of female extrapair mate choice8,9, one might speculate whether female song during the fertile period has a similar function2. Although it has been suggested repeatedly that females use calls to incite male–male competition to obtain copulations and sperm from the best available male10, the idea that female song can act as an invitation to obtain extrapair copulations from other higher quality males has received little attention2. In the alpine accentor (Prunella collaris ), female song attracts competing males from a multimale group but apparently no extragroup (or extrapair) males11. In an African estrildid species (Uraeginthus bengalus ), however, males react to female song with courtship and sexual behaviour, clearly illustrating that female song may be a sexual signal12. If females use song to attract and copulate with the ‘best’ male, its importance is likely to be underestimated, because it will probably occur most often at dawn immediately after egg laying (when females in most species have their peak fertility), at a time when the visibility is generally low and singing females may easily be mistaken for males. Although most of the observations described here are anecdotal, they do suggest that a mate TREE vol. 13, no. 8 August 1998
Reply from A.L.R. Thomas
Was Adrian Thomas’s short note in the last issue of TREE 1 intended to be provocative? The Cambrian explosion has not been ‘blown out of the water’. First, the existence of late Precambrian metazoan fossils does not alter the fact that Cambrian fossils record an explosive diversification of animals, although it may make it easier to explain. Second, it has been many years since the fossil record of metazoan animals started with the Cambrian explosion – I first learned about the late Precambrian Ediacara fauna when I was an undergraduate 25 years ago and it was not particularly new to science then. The recent discovery of fossilized metazoan embryos in 570 million-year-old Precambrian rocks in China2 is tremendously exciting, but it is not the first indication of a metazoan fossil record predating the Cambrian explosion. The Ediacara fauna (now known as Vendozoa or Vendobionta), once shoehorned into extant phyla, has been interpreted as representing an early radiation of metazoans3 that were not closely related to Cambrian metazoan animals and that flourished during the last 60 million years (very approximately) of the Precambrian but became extinct before the Cambrian explosion. The Chinese fossil embryos may represent the oldest fossils of metazoans that were directly ancestral to Phanerozoic (Cambrian onwards) lineages. A plausible explanation has been put forward (also reported in the same issue of TREE ) that the vendozoans occupied the ecological niches available to large animals (several cm), restricting Precambrian (late Proterozoic and Vendian) precursors of Phanerozoic metazoans to small size (mm) and, therefore, little chance of fossilization4. The Cambrian explosion can then be attributed partly to a size increase of ‘Phanerozoic Metazoa’ once the vendozoans became extinct. In terms of the fossil record of all metazoans, the vendozoans could even predate the latest Chinese findings. Recent dating of the Ediacara fauna of the English Midlands suggests that it has a minimum age of 603 ± 2 million years, although the authors5 are cautious about the accuracy of this figure. The fossil record has enough gaps in it – let’s not introduce more through forgetfulness!
Horne chides me for enhancing the gaps in the fossil record through ‘forgetfulness’ and for being provocative in ignoring the Precambrian Ediacara fauna. Space constraints aside, I claim two mitigating circumstances: First, both Bell1 and I reviewed the substantial evidence in favour of a long Precambrian history of the metazoans (e.g. widespread trace fossils and possible fossilized metazoan faecal pellets, and decline in stromatolite diversity and abundance from about 1000 million years ago onwards), and the most likely reason why they did not fossilize easily before the Cambrian (because atmospheric oxygen levels fell below a critical threshold for the formation of hard body parts) in TREE last year2. Second, the Ediacaran fauna are so enigmatic as to be uninformative. The Ediacaran fauna have been described as lichens3 or as an entirely separate experiment in multicellularity4, but recent analyses suggest that they might be nothing more exciting than fossils of conventional metazoans5,6. The argument over these fossils may be intense precisely because they are enigmatic. The Ediacaran sites I have visited in Sweden are striking for their beautiful preservation of the Precambrian sea floor, and for the astonishing abundance of trace fossils they contain, but the Ediacaran fossils (mostly Psammocoralia) are most impressive for their lack of discernible features. On the charge of being provocative, I claim no credit for that – the discovery of these fossils is in itself both exciting and provocative. These Precambrian metazoan embryo fossils at last provide a clear refutation of the idea that the Cambrian explosion represents the sudden emergence of all the metazoan phyla in a few short millions of years, and there is no longer any need to resort to anything other than conventional, gradual, progressive darwinian evolution to account for the origins of the metazoa. The Cambrian explosion is now clearly identified as a taphonomic event, marking the evolution (in only about two-thirds of the metazoan phyla) of features permitting fossilization. As Darwin7 predicted, and as a series of recent molecular analyses have confirmed8, the metazoa underwent a period of cryptic evolution before the Cambrian that was as long or longer than has elapsed since.
David J. Horne
A.L.R. Thomas
School of Earth & Environmental Sciences, University of Greenwich, Chatham Maritime, Kent, UK ME4 4TB ([email protected])
Dept of Zoology, University of Oxford, South Parks Road, Oxford, UK OX1 3PS ([email protected]) References
References 1 Thomas, A.L.R. (1998) Trends Ecol. Evol. 13, 129 2 Xiao, S., Zhang, Y. and Knoll, A.H. (1998) Nature 391, 553 –558 3 Seilacher, A. (1989) Lethaia 22, 229–239 4 Cooper, A. and Fortey, R. (1998) Trends Ecol. Evol. 13, 151–156 5 McIlroy, D., Brasier, M.D. and Moseley, J.B. (1998) J. Geol. Soc. Lond. 155, 401– 411
322
1 Bell, M.A. (1997) Trends Ecol. Evol. 12, 1–2 2 Thomas, A.L.R. (1997) Trends Ecol. Evol. 128, 44 – 45 3 Retallack, G.J. (1994) Paleobiology 20, 523 –544 4 Buss, L.W. and Seilacher, A. (1994) Paleobiology 20, 1– 4 5 Conway Morris, S. (1993) Nature 361, 219 –225 6 Fedonkin, M.A. and Waggoner, B.M. (1997) Nature 388, 868 – 871
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00
7 Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, Murray 8 Li, C-W., Chen, J-Y. and Hua, T-E. (1998) Science 279, 879 – 882
Female song for mate attraction: an overlooked phenomenon? In her recent TREE review, Langmore looked in detail at possible functions of female song in birds1. Although it is now generally accepted that males sing to attract females2,3, Langmore concludes that the attraction of mates does not appear to be a common function of female song. Here, we would like to draw attention to several observations that suggest that a mate attraction function of song might be more common in females than previously thought. First, Drent observed that female great tits (Parus major ), start singing after losing their mate, irrespective of whether they are inside or outside the territory of their former mate (P.J. Drent, PhD thesis, University of Groningen, 1983). He further observed that once females had obtained a mate again, spontaneous song declined almost completely. These observations suggest that female great tits use song to attract a new male. Second, in another tit species, the blue tit (Parus caeruleus ), Kempenaers and co-workers4 removed nine males for about one hour during the fertile period of their female, and they observed that all females started giving contact calls immediately and two of them also started singing, lending further support to the idea that females use song to attract their own or a new male. Third, Snow 5 also described that a female blackbird (Turdus merula ), started singing after having lost her male. Fourth, female canaries (Serinus canaria ), have been reported to sing frequently if they are kept isolated from males 6,7. Finally, knowing that male song is important in the context of female extrapair mate choice8,9, one might speculate whether female song during the fertile period has a similar function2. Although it has been suggested repeatedly that females use calls to incite male–male competition to obtain copulations and sperm from the best available male10, the idea that female song can act as an invitation to obtain extrapair copulations from other higher quality males has received little attention2. In the alpine accentor (Prunella collaris ), female song attracts competing males from a multimale group but apparently no extragroup (or extrapair) males11. In an African estrildid species (Uraeginthus bengalus ), however, males react to female song with courtship and sexual behaviour, clearly illustrating that female song may be a sexual signal12. If females use song to attract and copulate with the ‘best’ male, its importance is likely to be underestimated, because it will probably occur most often at dawn immediately after egg laying (when females in most species have their peak fertility), at a time when the visibility is generally low and singing females may easily be mistaken for males. Although most of the observations described here are anecdotal, they do suggest that a mate TREE vol. 13, no. 8 August 1998