© 1994 Nature Publishing Group
SCIENTIFIC CORRESPONDENCE
in the progenote. As information from
other genes of similar antiquity becomes
available, more clarity should ensue. It is
the data, rather than arguments, that are
lacking.
Ri.idlgerCerff, William Martin
Henner Brinkmann
Institut fUr Genetik,
Technische Universitat Braunschweig,
0-38023 Braunschweig, Germany
Can female adders
multiply?
SI R - Madsen et al. I conclude from a field
study on an adder (Vipera herus) popula-
tion from southern Sweden that most of
the females mated multiple times in a
season, and that those females that copu-
late more frequently than others also
produce a higher mean number of viable
offspring. These findings suggested to the
authors that the increase in viability of
fertilized eggs is due to sperm competi-
tion, in which the 'best' sperm compete for
the chance to effect fertilization. But in an
adder population from northeastern Italy
(Sella Nevea, Carnic Alps, 1,100 m high).
we find that only about 18% of the females
mated multiple times in a season, and
those females copulating multiple times
very often do so with the same male
2
.
In the reproductive period of 1993. we
captured 20 free-living adders (belonging
to the population studied by Luiselli2)
immediately after the end of hibernation
(before the start of the mating period),
and placed them in a outdoor enclosure
(in the adder habitat) to monitor the exact
number of copulations of each female.
Receptive males from the same popula-
tion were introduced into the enclosure.
Ten female individuals were mated only
once (group A), and ten were mated
multiple times (from 3 to 8, group B). We
used differently sized males, but there
were no mean size differences between
adders that copulated with female groups
A or B. After the end of the experiments.
we measured clutch parameters of the two
groups of females by using methods as
described in refs 3 and 4.
As in the study by Madsen et al. I, we
found that the number of copulations was
not significantly correlated with litter size
or with female fecundity relative to body
size (in either case, r < 0.3, P > 0.1). and
that the number of matings by a female did
not affect her mcan offspring mass, her
total mass or her proportional body mass
loss during gestation (in all cases, r < 0.3 ,
P > O. I) . But our data did differ from
those of Madsen et al. I in that multiple
matings did not reduce the proportions of
offspring that were dead at birth. In fact.
the proportion of dead offspring per litter
was not significantly different in the two
groups of females (x = 12.0 ± [s .d.]
528
16.52% of female group B versus 14.0 ±
17.66 % of female group A: two-tailed
t = - 0.19, d.f. = 18, P> 0.8) , and the
correlation between proportion of still-
born young and number of different males
mated with was not significant (r = 0.53,
ANOYA: mean square = 0.069, F= 3.17,
P = 0.1). Thus, at least in the population
we studied, the number of different males
mated with does not seem to be the
primary determinant of the proportion of
viable offspring produced by a female
adder. Thus, although the arguments of
Madsen et al. I are interesting, we suspect
their results may not apply to all adder
populations. On the other hand, it could
be claimed that the mating pattern is
adaptive in each case, and that female
adders mate multiply with different males
only when there is a positive benefit from
doing so.
Massimo Capula
Luca Luiselll
Department of Animal and Human Biology,
University of Rome "La Sapienza",
via Alfonso Borelli 50 ,
/-00161 Rome, Italy
SIR - Females of many animal species
mate frequently, with several different
males. This 'promiscuous' female be-
haviour is unexpected from simple Darwi-
nian theory because the number of
offspring produced by a female does not
increase if she has more sexual partners.
In an earlier paperl, some of us suggested
that by this behaviour, females promote
sperm competition among males, and
their offspring are thereby sired by males
with 'better' genes. We found that female
adders (Vipera herus) that mated with
several males produced a higher propor-
tion of viable offspring than did 'monoga-
mous' females I. Parker' suggested that
judgement of this hypothesis should be
suspended until further evidence was
accumulated. Here we report a study of
lizards that strongly supports the earlier
hypothesis I. Not only docs multiple mat-
ing of lizards with different partners
increase hatching success and lower
the incidence of deformities, but it also
enhances survivorship of free-living
juveniles.
We studied a population of marked,
blood-sampled sand lizards (Lacerta aKi-
lis) 50 km south of Gothenburg on the
Swedish west coast
h
.
7
. Matings were
directly observed (11=32) or were inferred
from the post-copulatory mate guarding
(11= 108) that characteristically follows the
2-4-min-long copulation
7
. In 1989 and
1990 , we incubated eggs from the female
lizards under identical conditions in the
laboratory. Hatchlings were marked by
toe-clipping and were blood sampled be-
fore being released at random sites at the
Asketunnan study area. We used DNA
fingerprinting7 to establish paternity and
to assess the degree of genetic variation in
the population. After one year we recap-
tured the survivors to determine whether
offspring from multiply-mating females
were more likely to survive as free-living
juveniles.
Genetic variation in the population was
low (mean band sharing among indi-
viduals was 66 %., range, 63-68, 11=30).
Despite the low genetic variation, we
could identify male-specific bands in five
broods; four had mixed paternity (our
unpublished data). Females mated on
average 3.7 times with 1-5 different males
(mean, 1.7). The resulting clutches varied
in hatching success (mean, 81 'Yo ; range,
38-1(0). We recaptured 42 of the 516
released hatchlings, with some clutches
being much more highly represented than
others (mean , 9.5%; range, 0-43%). As
some of us predicted (one-tailed tests), a
female's number of sexual partners was:
(1) positively correlated with the hatching
success of her eggs (",=0.59, P=O.0003.
11=31); (2) negatively correlated with the
proportion of hatched young that exhi-
bited malformations (r,=O.33, P=0.035 ,
11=31); and (3) positively correlated with
the proportion of her offspring that we re
recaptured after I year (r, =0.37,
P=().020, 11 = 31). This result remained
significant when clutch size was controlled
for in a partial correlation analysis
(r,=().41, P=O.OI4, 11=31).
Could these differences in offspring
viability be caused by nutrients in the
ejaculate, rather than by genetic enhance-
ment of offspring" Probably not. Some
females mated more than once with the
same male, enabling us to examine the
effects of number of copulations indepen-
dently of the number of partners. In-
creased copulations with the same male
did not increase a female's offspring
viability (number of matings versus hatch-
ing success: r, = -0.19, P=O.502; versus %
deformities: r, =().42. P=0.136; versus
offspring survival: r,=O.41, P=O.143,
11= (5).
Mats Olsson*
Department of Zoology,
University of G6teborg,
S-413 90 G6teborg, Sweden
Annlca Gullberg
Hakan Tegelstrom
Department of Genetics,
Uppsala University,
S-750 07 Uppsala, Sweden
Thomas Madsen
Richard Shine
School of Biological Sciences,
The University of Sydney,
NSW 2006, Australia
"Present address as for T.M. and R.S .
1. Madsen, r. etat, Nature 355, 440-441
(1992 ).
2. Lui selli,l.Acta oecol. (in the press).
3. Capula. M , et at, Vie et Milieu 42. 327-336
(1992),
4. LuiseliLl. Oikos64, 601··604 (1992).
5. Parker. G, Nature 355, 395- 396 (1992).
6. Olsson, M, the sis, Univ. Gothenburg (1992).
7. Olsson. M. et al. Anim. 8ehav. (in the press).
NATURE . VOL 369 . 16 JUNE 1994