CORRESPONDENCE
7 Darwin, C. (1859) On the Origin of Species by
Cambrian explosion still in
the water
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!
David J. Horne
School of Earth & Environmental
Sciences, University of Greenwich,
Chatham Maritime, Kent, UK ME4 4TB
(d.j.horne@greenwich.ac.uk)
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 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00
Reply from A.L.R. Thomas
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.
A.L.R. Thomas
Dept of Zoology, University of Oxford,
South Parks Road, Oxford, UK OX1 3PS
(adrian.thmas@zoology.ox.ac.uk)
References
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
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

attraction function of female song might be more
widespread than is currently realized because it
can be easily overlooked. As stressed by
Langmore, the key questions are now:
• Why is there so much variation in singing
frequency between females of a given species,
and what are the fitness consequences of
this variation?
• Why is there so much variation among species
in the incidence of female song?
• Why do females in some species use calls and
in others use song to fulfil apparently similar
functions?
Only carefully designed experiments, time
consuming observations and comparative studies
will be able to answer these questions.
Reply from N.E. Langmore
Although female song for mate attraction could well
be more widespread than is currently thought, the
examples presented by Eens and Pinxten highlight
the difficulties of inferring function in the absence
of detailed, experimental studies. For example, in
the experimental study they refer to, two out of
nine female blue tits sang after their mates had
been removed, suggesting that they were singing
to attract a new mate. However, three of these
nine females were also reported to engage in
fights with neighbouring females1. As blue tits are
facultatively polygynous1, it is equally plausible
that female song in this species could function in
Shortening the
phylogenetic fuse
Cooper and Fortey recently argued in TREE 1 that
spectacular evolutionary radiations documented in
the fossil record – such as the Cambrian and
Tertiary ‘explosions’ – are preceded by long
periods of cryptic evolution where major
morphological innovations are established in small
poorly-preserved ancestors – the ‘phylogenetic
fuse’. Evidence for this came from a variety of
molecular studies: for instance, the extensive
genetic differences between metazoan phyla imply
that they diverged long before their first fossil
appearances in early Cambrian strata2.
A reanalysis of the molecular evidence challenges
this estimate, and suggests a much more recent
divergence time of 600–670 (rather than 1200)
million years BP (Ref. 3). Even these revised dates,
however, imply a substantial period of cryptic
evolution before the Cambrian explosion of
550 million years ago.
While it was admitted that ‘the period of earlier
phylogenesis would be overestimated if rates of
molecular evolution were considerably accelerated
during large radiations’, this scenario was largely
dismissed1. However, this hypothesis deserves
serious consideration. A recent study4 has
demonstrated that morphological and molecular
rates of evolution are highly correlated, across a
variety of groups and a wide range of morphological
TREE vol. 13, no. 8 August 1998
CORRESPONDENCE
Marcel Eens
Rianne Pinxten
Dept of Biology, University of Antwerp,
UIA, Universiteitsplein 1,
B-2610 Wilrijk, Belgium
(eens@uia.ua.ac.be)
References
1 Langmore, N.E. (1998) Trends Ecol. Evol. 13,
136 –140
2 Catchpole, C.K. and Slater, P.J.B. (1995) Bird
Song: Biological Themes and Variations,
Cambridge University Press
3 Eens, M. (1997) Adv. Stud. Behav. 26, 355 – 434
female–female aggression, as has been observed
in many other facultatively polygynous species2,
rather than for mate attraction. It would be
interesting to know if the female songs described
in the other studies were also associated with
female–female aggression. Although the
possibility that females sing to attract extra-pair
males is intuitively appealing, an experimental
study of female song in the species with the
highest incidence of extra-pair paternity failed to
find any support for this hypothesis3. I agree
with Eens and Pinxten that more experimental
studies are needed to differentiate between the
possible functions of female song. In particular,
before we can conclude that female song
functions for mate attraction we need to know that
males can distinguish between male and female
and genetic traits. Rapid morphological change
appears to be accompanied by rapid molecular
change. Thus, the unexpectedly large genetic
differences between metazoan phyla (or
mammalian orders) might document a relatively
short period of accelerated genetic evolution in the
late Precambrian (or early Tertiary), rather than
(implausibly) long intervals of normal genetic
change. This rate variability will probably not
eliminate altogether the inferred period of cryptic
evolution; genetic changes would have to be very
greatly accelerated for this to happen1. However, it
will help to further shorten this phylogenetic fuse to
a length that is acceptable to most palaeontologists.
Correlated rates of morphological and
molecular evolution would explain why molecular
estimates for divergence times are consistently
greater than well-supported palaeontological
estimates. Indeed, these dating discrepancies
constitute strong evidence for Omland’s proposals4.
Michael S.Y. Lee
Dept of Biological Sciences,
Monash University, Clayton,
VIC 3168, Australia
References
1 Cooper, A. and Fortey, R. (1998) Trends Ecol.
Evol. 13, 151–156
2 Wray, G.A., Levinton, J.S. and Shapiro, L.M.
(1996) Science 214, 568 –573
3 Ayala, F.J., Rzhetsky, A. and Ayala, F.J. (1998)
Proc. Natl. Acad. Sci. U. S. A. 95, 606 – 611
4 Omland, K.E. (1997) Evolution 51, 1381–1393
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00
4 Kempenaers, B. et al. (1995) Behav. Ecol.
Sociobiol. 36, 33 – 42
5 Snow, D.W. (1958) A Study of Blackbirds, Oxford
University Press
6 Pesch, A. and Güttinger, H-R. (1985) J. Ornithol.
126, 108 –110
7 Vallet, E. et al. (1996) Ethology 102, 617– 628
8 Eens, M. et al. (1991) Behaviour 116, 210 –238
9 Hasselquist, D. et al. (1996) Nature 381,
229 –232
10 Montgomerie, R. and Thornhill, R. (1989)
Ethology 81, 209 –220
11 Langmore, N.E. et al. (1996) Proc. R. Soc.
London Ser. B 263, 141–146
12 Gahr, M. and Güttinger, H-R. (1986) Ethology 72,
123 –131
songs, and that they are preferentially attracted to
female songs.
N.E. Langmore
Dept of Zoology, University of
Cambridge, Downing Street, Cambridge,
UK CB2 3EJ (nel10@hermes.cam.ac.uk)
References
1 Kempenaers, B. et al. (1995) Behav. Ecol.
Sociobiol. 36, 33 – 42
2 Langmore, N.E. (1998) Trends Ecol. Evol. 13,
136 –140
3 Cooney, R. and Cockburn, A. (1995) Anim. Behav.
49, 1635 –1647
Reply from A. Cooper and
R. Fortey
While Lee agrees that a phylogenetic fuse – an
extended, but cryptic, period of evolution – must
have preceded the explosive radiations at the
beginning of both the Cambrian and Tertiary, he
questions whether molecular data might
overestimate its length. In our review1 we noted
that the recent claims of a shortened Precambrian
‘fuse’2 did not affect our conclusions, and
subsequently published3 and submitted work
further supports unexpectedly early divergences
within metazoa, mammals and birds.
We also discussed the contention that periods
of rapid morphological change might be
associated with accelerated rates of molecular
evolution and suggested this possibility deserved
more study. However, we point out that, in addition
to lacking a suitable genetic mechanism, relative
rate tests performed on the Cambrian and early
Tertiary data detect no such acceleration. To
explain this finding, a simultaneous acceleration of
similar magnitude would be required in the
mitochondrial and nuclear genes of the sister taxa
to metazoa, and birds and mammals (other
eukaryotes, and reptiles, respectively).
Furthermore, for molecular rates to be
anomalously high during the early Cambrian and
Tertiary, it would be necessary to propose that
subsequent morphological radiations in the history
323