ANIMAL BEHAVIOUR, 2001, 62, 427?433
doi:10.1006/anbe.2001.1790, available online at http://www.idealibrary.com on
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abnormally low reproductive output with a first partner should act as a strong stimulus for females to
accept sperm from a new male. To test this prediction in a naturally polyandrous, sperm-storing,
viviparous species, we restricted female Cordylochernes scorpioides pseudoscorpions to mating with a single
male and then gave them the opportunity to remate with a different male after their first brood of
embryos either aborted spontaneously, was experimentally removed, or was successfully carried to term.
With complete brood failure presumably providing the strongest possible cue to females of a poor-quality
first mate, the trading-up hypothesis would predict that females that aborted their first brood should have
been significantly more sexually receptive than females that had produced a successful first brood.
Instead, they were significantly less receptive. Furthermore, none of the sexually unreceptive, spon-
taneously aborting females produced a successful second brood, indicating that C. scorpioides females that
copulate with a single male may become locked into cycles of brood failure followed by sexual
unreceptivity. Our findings suggest that the negative impact of abortion on female sexual receptivity may
place physiological constraints on the ability of viviparous females to use polyandry as a facultative
mating strategy for improving on a bad first mate.
? 2001 The Association for the Study of Animal Behaviour
Females of many species mate with more than one male
and may derive a variety of material benefits from engag-
ing in such polyandrous behaviour (e.g. Gwynne 1984;
Hoogland 1998; Ivy et al. 1999). Alternatively, the ben-
efits to polyandry may be genetic (e.g. Tregenza & Wedell
1998). In socially monogamous birds, molecular genetic
evidence of extrapair paternity has led to the hypothesis
that polyandry is a facultative mating strategy that
depends on the genetic quality of a female?s ?social mate?.
According to this ?trading-up? hypothesis, females may
often engage in extrapair copulation with a superior male
in order to compensate for a breeding partner of relatively
poor quality (Wetton & Parkin 1991; Kempenaers et al.
1992; Hasselquist et al. 1996; Petrie & Kempenaers 1998).
The trading-up hypothesis thus makes the clear predic-
tion that the production of poor-quality offspring, abnor-
mally low reproductive output, or complete reproductive
In viviparous species, reproductive failure is manifested
as spontaneous abortion, a common but poorly under-
stood phenomenon (Hertig & Rock 1959; Hertig et al.
1959; Alberman 1988; Hill 1995; Valhe? et al. 1999).
Testing the trading-up hypothesis in viviparous females
that store sperm and can therefore potentially ?mate for
life? provides an excellent opportunity to investigate the
causal relationship between abortion and polyandry. Has
spontaneous abortion resulting from embryonic inviabil-
ity driven the evolution of polyandry (Zeh & Zeh 1996,
1997; Newcomer et al. 1999), or has the evolution of
polyandry made selective/differential abortion available
to viviparous females as an adaptive strategy for maximiz-
ing the genetic quality of their offspring (Birkhead &
M?ller 1998; M?ller 1998)? Unfortunately, investigating
the causes and consequences of abortion is seriously
hampered in most viviparous animals precisely becauseSpontaneous abortion depresse
viviparous
JEANNE A. ZEH
Department of Biology and Program in Ecology, Evoluti
(Received 26 January 2000; i
final acceptance 8 February
The ?trading-up? hypothesis for polyandry, which p
means of improving on the quality of their firs
explanation for mixed paternity in socially monfailure with a first partner should stimulate females to
copulate with a different male.
Correspondence: J. A. Zeh, Department of Biology and Program in
Ecology, Evolution and Conservation Biology, University of Nevada,
Reno, NV 89557, U.S.A. (email: jaz@unr.edu).
0003?3472/01/090427+07 $35.00/0 427female sexual receptivity in a
rthropod
DAVID W. ZEH
and Conservation Biology, University of Nevada, Reno
ial acceptance 7 April 2000;
01; MS. number: A8704R)
ts that females copulate with additional males as a
ating partner, has been proposed as a general
amous birds. As a corollary of this hypothesis,embryos develop within the female and the intrusive
and/or technologically complex methods required to
diagnose abortion render its study impracticable. By con-
trast, spontaneous abortion, particularly of entire broods,
is easily diagnosed in pseudoscorpions. Females nourish
developing embryos in a translucent, external brood sac
? 2001 The Association for the Study of Animal Behaviour
induced brood abortion acting to suppress rather than
428 ANIMAL BEHAVIOUR, 62, 3stimulate female sexual receptivity towards a different
male. Taken together with previous findings, our results
suggest that polyandry in C. scorpioides is a pre-emptive
mating strategy for minimizing the impact of potentially
costly abortions on female reproductive success.
Biology of Cordylochernes scorpioides
Distributed throughout the rain forests of Central and
South America (Beier 1948), C. scorpioides inhabits decay-
ing trees in the families Moraceae and Apocynaceae. The
pseudoscorpions gain access to these rich but patchily
distributed and ephemeral habitats by hitchhiking under
the elytra of the giant harlequin beetle, Acrocinus longi-
manus (Zeh & Zeh 1992). Because of this obligate associ-
ation, pseudoscorpion colonization is restricted to the
brief period when newly fallen or dying trees attract
beetles for mating and oviposition (Zeh et al. 1992b).
Populations in dead trees remain marooned for several
generations until beetle larvae complete development
and the pseudoscorpions can climb on board new adult
harlequins to disperse en masse. This novel mode of dis-
persal has been exploited by males that fight to monop-
olize beetle abdomens as strategic sites for intercepting
and inseminating dispersing females (Zeh & Zeh 1992).
DNA profiling has demonstrated a strong, positive corre-
lation between male size and reproductive success during
the pseudoscorpion?s dispersal phase on beetles (Zeh et al.
1997). However, this intense selection is undermined by
polyandry and sperm storage by females. After dispersal,
the majority of females produce mixed-paternity broods
sired by up to four males (Zeh et al. 1997). Evidenceoverlying the genital opening (Weygoldt 1969). This
form of viviparity makes it possible to accurately assess
gravidity and subsequent spontaneous abortion.
Here, we exploit the unique features of pseudoscorpion
reproductive biology in a study designed to investigate
the potential constraints on trading-up in a sperm-
storing, viviparous species. In the harlequin beetle riding
pseudoscorpion, Cordylochernes scorpioides, females can
store sperm indefinitely (Newcomer et al. 1999) and
acquiring sperm from more than one male prior to
offspring production is an active mating strategy. Females
recognize and discriminate against previous mates, pre-
ferring instead to accept sperm from different males (Zeh
et al. 1998). If experimentally restricted to multiple
inseminations by a single male, females suffer a signifi-
cantly higher rate of spontaneous abortion compared
with females accepting the same quantity of ejaculate
from two different males (Newcomer et al. 1999). In the
experiment reported here, all females were restricted to
mating with a single male and were then given the
opportunity to engage in polyandry after their first brood
either aborted spontaneously, was experimentally
removed, or was successfully carried to term. The pattern
of sexual receptivity shown by these females was found to
be the opposite of that predicted by the trading-up
hypothesis, with both spontaneous and experimentallysuggests that many of these offspring are sired by males
that females had mated with before boarding beetles todisperse. Polyandry and prolonged sperm storage may
therefore enable smaller males to circumvent the bottle-
neck of dispersal-generated sexual selection and thereby
transmit their genes to future tree populations.
As invertebrates that are both polyandrous and vivi-
parous, these pseudoscorpions possess a suite of repro-
ductive and behavioural traits that makes them highly
amenable to investigation of the proximate mechanisms
and evolutionary causes of polyandry in the context of
viviparity. Sperm transfer is indirect via a spermatophore
deposited on the substrate. The spermatophore consists
of a stalk, a ball of fluid, and, at the apex of the stalk, a
complex, folded, tubular packet containing the sperm
(Weygoldt 1969). Mating involves a well-defined
sequence of behaviours in which the male grasps the
female while he constructs and deposits a spermatophore.
After spermatophore deposition, the male manoeuvres
the female into a position where the sperm packet
directly contacts her gonopore. Successful attachment of
the sperm packet to the gonopore is associated with a
pronounced abdominal flexure by the female (Zeh & Zeh
1994). This flexure presses the sperm packet down
onto the ball of fluid, causing a long, hooked tube
to evert from the packet into the female?s genital
aperture, followed by evacuation of sperm into her
reproductive tract.
This indirect method of sperm transfer makes female
cooperation essential for successful insemination (Zeh
1997). Females typically accept only the first of two or
more sperm packets deposited by a male during a single
mating event (Zeh 1997; Zeh et al. 1998). Unreceptive
females engage in one of several behaviours to block
sperm transfer. In some cases, females aggressively resist
the male and terminate mating by breaking free from the
male?s grasp before he initiates construction of a sper-
matophore. Alternatively, females occasionally refuse to
remain stationary during spermatophore deposition, forc-
ing the male to move and lose contact with the still
incomplete spermatophore. Finally, in the majority of
cases, the female cooperates with the male throughout
the entire period of spermatophore construction and
deposition, only to resist being pulled forward over the
sperm packet (Zeh 1997). The combination of external
spermatophore deposition and diagnostic female
behaviour provides a unique, noninvasive window
on mating event characteristics, such as the number of
spermatophores accepted and rejected by a female.
In pseudoscorpions, egg membranes rupture early in
development and individual embryos use a specialized
mouth precursor (the pumping organ) to actively draw
nutritive fluid, consisting of phospholipids, proteins and
polysaccharides, from the mother?s reproductive tract
(Weygoldt 1969). Embryos develop in a translucent brood
sac overlying the female?s genital aperture and develop-
ment can be easily monitored with minimal disturbance
to mother or embryos. This ?external-womb? form of vivi-
parity circumvents the technical difficulties of diagnosing
spontaneous abortion in other viviparous species such as
mammals. After becoming gravid, C. scorpioides females
use frass and silken threads to construct a brood nest.
Embryos require approximately 14 days to complete
males and females randomly. It was necessary to carry out
a large number of single-male matings to obtain a statisti-
they
fem
mb
cep
429ZEH & ZEH: CONSTRAINTS ON FACULTATIVE POLYANDRYcally sufficient number of cases of spontaneous brood
abortion for the aborted-first-brood category of females in
this experiment. After mating, we maintained females
individually in transparent, plastic vials containing nat-development, and birth occurs when the embryos rupture
the brood sac and emerge as protonymphs (see Weygoldt
1969). After birth, nymphs remain in the nest for approxi-
mately 2 days until they are fully sclerotized (Zeh 1997).
METHODS
Virgin males and females for this study were the
laboratory-reared offspring of 31 field-inseminated
females collected in December 1996 from large popu-
lations inhabiting three decaying Ficus trees in the former
Canal Zone of the Republic of Panama. Previous research
involving both multilocus and single-locus DNA profiling
has demonstrated that such tree populations are
founded by highly genetically diverse breeding groups of
unrelated individuals (Zeh et al. 1992a, 1994, 1997).
Levels of heterozygosity within large tree populations do
not differ significantly from heterozygosity estimates
based on random samples of individuals collected
from multiple trees (Zeh et al. 1994, 1997; D.W. Zeh,
unpublished data).
After birth, nymphs were reared individually, as
described elsewhere (Zeh & Zeh 1994). On attaining
sexual maturity, we allowed virgin females (N=228) from
each of these families to mate with a single, virgin male.
To avoid possible confounding effects of inbreeding
depression, no matings were carried out between full
siblings or half-siblings. With this exception, we paired
Table 1. Level of sexual receptivity in females 24 h after
successfully gave birth to nymphs (successful-first-brood
(experimental-removal females)
Female category
Nu
re
Aborted-first-brood females
Successful-first-brood females
Experimental-removal females
Fisher?s exact test: N=64, P=0.00005.urally produced Ficus frass, and fed them 8?10 late-instar
we removed protonymphs from the brood nest
immediately after birth and counted them.To evaluate the effect of reproductive outcome with
first mating partner on the propensity of females to accept
sperm from a second male, approximately 24 h after
either first-brood spontaneous abortion or the birth of the
first brood of nymphs, we allowed aborted-first-brood
females (N=21) and a random sample of successful-first-
brood females (N=23) the opportunity to remate with a
new male. For each of the two first-brood categories, we
initiated replications by placing the female with a ran-
domly chosen, nonsibling male in a 28-mm diameter
mating arena. We videotaped interactions using a Super
VHS camcorder for 30 min under red, fibre-optics illumi-
nation. We then transcribed the videotape of each mating
to determine the number of spermatophores deposited
and the number of sperm packets successfully transferred
by the male to the female. We assessed the influence of
first-brood abortion and postabortion sexual receptivity
on subsequent female reproductive success by monitoring
aborted-first-brood females for 35 days following their
remating opportunity, as described above.
To investigate whether abortion per se influences
female sexual receptivity rather than some unknown
correlate of abortion, such as poor female condition, we
carried out a manipulative experiment in which we ran-
domly selected gestating females (N=20) carrying late-
stage embryos (8?11 days after brood sac production) for
brood sac removal (?experimental-removal? females). In
this pseudoscorpion, a fine tube connects the embryos
developing within the external brood sac to the mother?s
reproductive tract. Gestation can be experimentally ter-
minated with minimal disturbance to the female by
gently lifting the brood sac from the female?s abdomen,
thereby severing the connecting tube. Twenty-four hours
after brood sac removal, we gave each female the oppor-
tunity to remate, as described above. We then transcribedTribolium confusum larvae per week. We monitored female
reproductive status every 3?4 days until brood sac pro-
duction, and then once per day thereafter. Since females
generally construct their brood nests on the walls of their
vials and embryonic development within the brood sac is
readily visible with the naked eye, it was possible to
monitor females and embryos with minimal disturbance.
A female was categorized as having suffered spontaneous
abortion of her entire brood if her brood sac detached
prematurely from her abdomen and no protonymphs
were born. For females whose first brood was successful,
videotapes of the matings to assess female sexual
receptivity.
RESULTS
Level of sexual receptivity in the successful-first-brood
category was very high, with 20 of the 23 females (87%)
accepting a sperm packet 24 h after giving birth to
nymphs (Table 1). Interestingly, of the three females that
were sexually unreceptive, two had given birth to very
few nymphs (six and eight nymphs). These broods sizes
were more than one standard deviation below the meanaborted their first brood (aborted-first-brood females),
ales), or had their brood sacs experimentally removed
er of sexually
tive females
Number of sexually
unreceptive females
7 14
20 3
6 14number of nymphs born to females in the successful-first-
brood category (X
SD=39
25, N=23). By contrast,
difference was highly significant (Fisher?s exact test:
430 ANIMAL BEHAVIOUR, 62, 3N=44, P=0.0005). The low rate of sperm transfer to the
aborted-first-brood females could not be attributed to lack
of sexual stimulation in males. The mean number of
spermatophores deposited by males placed with aborted-
first-brood females (X
SE=1.76
0.19) did not differ
significantly from that deposited by males placed
with successful-first-brood females (1.83
0.15, Mann?
Whitney U test: U=239, N1=21, N2=23, P=0.949). Fur-
thermore, in 12 of the 14 replications of the aborted-first-
brood female category in which no sperm transfer
occurred, the male deposited at least one spermatophore,
but the female refused to be pulled over it. In the
remaining two replications, the males attempted to
initiate copulation but were thwarted by the aggressive
behaviour of the females.
In the 35 days following the remating opportunity, one
of the 14 sexually unreceptive females in the aborted-
first-brood category died and the remaining 13 either
produced a second brood sac of embryos, which subse-
quently aborted (N=6), or did not produce another brood
sac (N=7). To test whether sexually unreceptive first-
brood females became receptive with time, the latter
females (N=7) were given a second opportunity to remate
14 days after aborting their first brood. All seven females
were once again found to be sexually unreceptive. Of the
seven aborted-first-brood females that had accepted a
sperm packet in their second mating, three successfully
gave birth to nymphs and four produced a second brood
sac that aborted.
The level of sexual receptivity displayed by females
whose brood sacs had been experimentally removed did
not differ significantly from that of females whose broods
had aborted naturally (Fisher?s exact test: N=43,
P=1.000), with six of 20 females (30%) accepting a sperm
packet (Table 1). Once again, the low rate of successful
sperm transfer in these matings could not be attributed
to male effects. The mean number of spermatophores
deposited by males mated to experimental-removal
females (1.90
0.19) did not differ significantly from that
deposited by males in the other two categories (Kruskal?
Wallis ANOVA: H61=0.111, P=0.946), and, in each of the
14 replications in which the female was sexually unrecep-
tive, the male deposited at least one spermatophore.
Unlike females in the spontaneously aborting category,
the majority of females in the experimental-removal
group (17 of 20) went on to produce a second brood sac
within 14 days of first-brood abortion. It was therefore
not possible to give experimental-removal females a
second remating opportunity, since gravid females are
incapable of accepting sperm and are thus invariably
sexually unreceptive.
DISCUSSION
The results of this study demonstrate that singly matedlevel of sexual receptivity in the aborted-first-brood cat-
egory of females was low, with only seven of the 21
females (33%) accepting a sperm packet (Table 1). ThisC. scorpioides females that have experienced brood
abortion remain sexually unreceptive, in marked contrastto females that have carried broods to term. Within 24 h
of successfully giving birth to nymphs, 87% of females
accepted sperm from a new male. This level increased to
95% when three females that had given birth to abnor-
mally small broods (4, 6 and 8 nymphs) were excluded
from the analysis. By contrast, the level of sexual recep-
tivity in females whose brood of embryos had spon-
taneously aborted was significantly lower, with only 33%
accepting sperm. Because unreceptive C. scorpioides
females do not generally reveal their unwillingness to
accept sperm until after the male has deposited a sper-
matophore, it was possible to eliminate differences in
male sexual motivation as a possible explanation for
differences in rate of sperm transfer to aborting and
nonaborting females. Furthermore, randomly selected
females whose brood sacs had been experimentally
removed were as sexually unreceptive 24 h after brood sac
removal as females whose broods had aborted naturally.
It thus seems likely that the low level of sexual receptivity
displayed by the spontaneously aborting females was the
result of embryo abortion per se rather than a conse-
quence of poor female condition. Unfortunately, sexual
receptivity of the experimental-removal females could
not be tested through time, and it was therefore not
possible to completely eliminate the ?poor female quality?
hypothesis. However, we have shown elsewhere that,
when females are given the opportunity to mate with
more than one male prior to first brood production, they
suffer a significantly reduced rate of spontaneous abor-
tion compared with females restricted to multiple insemi-
nations by a single male (Newcomer et al. 1999). Poor
female quality could therefore provide at best only a
partial explanation for the results reported here.
While the precise mechanisms through which abortion
depresses sexual receptivity remain to be determined,
it seems likely that, in these viviparous females, the
endocrine balance required for nourishing broods of
developing embryos differs significantly from that of
nongestating females. Our results suggest that, when
broods are successfully carried to term, birth of the
nymphs acts as a switch, triggering a change in maternal
hormone production, a return to nongestation concen-
tration levels, and a reinstatement of sexual receptivity.
Without such a switch, the hormone balance of aborting
females remains set up for nourishing embryos and serves
as a block to remating. In mammals, both recurrent
spontaneous abortion (Bussen et al. 1999) and low female
libido (Petty 1999) are known to be associated with
abnormalities in the secretion of the pituitary hormone
prolactin. In invertebrates, female sexual receptivity has
been linked to levels of both dopamine (Neckameyer
1998) and juvenile hormone (Kerr et al. 1997; Schal et al.
1997) but, to our knowledge, the consequences of spon-
taneous abortion for hormone balance and female sexual
receptivity have not been investigated.
With complete brood failure presumably providing the
strongest possible cue to females of a poor-quality first
mating partner, the trading-up hypothesis would predict
that females in the aborted-first-brood category of this
study should have been significantly more receptive to
receiving sperm from a different male than females that
431ZEH & ZEH: CONSTRAINTS ON FACULTATIVE POLYANDRYhad produced a successful first brood. Instead, they were
significantly less receptive. Furthermore, by refusing to
accept sperm from a different male, these females failed
to take advantage of the opportunity to potentially
improve their future reproductive success. With none of
the sexually unreceptive, aborted-first-brood females
bringing a second brood successfully to term, our findings
indicate that C. scorpioides females that mate with only
one male prior to producing their first brood run the risk
of becoming locked into a cycle of brood failure followed
by sexual unreceptivity.
In this experiment, males were randomly allocated to
females as first mates. It might therefore be argued that
the results reported here do not provide a legitimate test
of the trading-up hypothesis because virgin experimental
females were deprived of the opportunity to exercise
choice and reject nonpreferred males. The experimental
design may thus have exposed females to a risk of spon-
taneous abortion that is never experienced under natural
conditions. Several lines of evidence suggest that this
criticism is invalid in the context of the mating behaviour
of C. scorpioides females. In this pseudoscorpion, as in
many other animal species, females encounter potential
mates in a sequential fashion and do not have the
opportunity to simultaneously evaluate a range of male
phenotypes (Zeh et al. 1998). Under such conditions, a
female must assess the current male against either an
internal standard or her memory of males previously
encountered (Gabor & Halliday 1997). Sequential mate
choice is thus an iterative decision-making process in
which a female must repeatedly choose whether to mate
or not to mate. Our previous research has shown that
C. scorpioides females are almost invariably sexually recep-
tive as virgins but exercise choice at second mating when
they discriminate against previous mates and preferen-
tially accept sperm from different males (Zeh et al. 1998).
In a study that involved large sample sizes, multivariate
morphometric analyses and a measure of male sexual
performance, we were unable to detect any evidence of
female mate choice based on phenotypic indicators of
inherent male genetic quality (Zeh et al. 1998). Further-
more, as described above, C. scorpioides females have com-
plete control over sperm transfer and cannot be coerced
into accepting sperm packets from males (Zeh et al.
1998). In the study reported here, females were experi-
mentally precluded from engaging in polyandry prior to
first brood production. However, as virgin individuals,
they were not deprived of their usual opportunity to
exercise choice in whether or not to accept sperm. At a
more general level, it should also be pointed out that
constraints on mate choice provide the very basis for the
trading-up hypothesis. Polyandry is hypothesized to
result from ecological or social factors that constrain
females into accepting less-than-optimal first mates.
The pattern of female sexual receptivity revealed by this
study suggests that polyandry in this pseudoscorpion is
not a facultative mating strategy in which females use low
reproductive success with a first mating partner as a cue
for remating with a different male in order to acquire
more viable paternal genes for their offspring. Indeed,
the negative impact of abortion both on a female?sreproductive success and on her subsequent propensity
to remate strongly suggests that C. scorpioides females
should avoid abortion, rather than using it as a means of
optimizing the genetic quality of their offspring. Else-
where, we have shown that C. scorpioides females signifi-
cantly reduce the rate of total brood abortion by mating
with more than one male before fertilizing any eggs (Zeh
1997; Newcomer et al. 1999). In an experiment that
controlled for male mating experience and the amount of
ejaculate received, females that acquired sperm from two
different males prior to producing their first brood
reduced their rate of total brood abortion by 33%, thereby
increasing their lifetime reproductive success by 32%,
compared with females mated twice to a single male
(Newcomer et al. 1999). Reduction in spontaneous abor-
tion rate through polyandry could result from reduction
in the rate of fertilization of eggs either by genetically
incompatible sperm or by sperm carrying intrinsically
inferior haploid genomes, incapable of successfully sup-
porting embryonic development. If poor genetic quality
of males and/or sperm were the primary cause of embryo
failure, the reproductive consequences of mating with a
particular male should be consistent across females. How-
ever, in a study in which 67 males were each mated to
two females, the numbers of nymphs born to each male?s
two mates were completely uncorrelated (Zeh 1997).
Broods of both females failed for only two of the 67
males, whereas, for 25 males, mating resulted in complete
brood failure in one female but successful nymph produc-
tion in the other. Given this absence of consistent effects
of male genotype on female reproductive success, the
enhanced reproductive success of polyandrous females
appears most consistent with the genetic incompatibility
avoidance hypothesis.
The generality of the findings reported here is at
present unclear, since the impact of spontaneous abor-
tion on female sexual receptivity remains to be investi-
gated in other viviparous species. None the less, our
results do suggest that trading-up as a female mating
strategy, although supported by studies of several bird
species (Petrie & Kempenaers 1998; Jennions & Petrie
2000), may be under greater constraints in viviparous
species. Live-bearing females differ from egg-laying
females in two important respects. First, viviparity is
likely to make females particularly vulnerable to repro-
ductive loss through genetic incompatibility, because the
development of the embryo within the mother creates
potential for genomic-conflict-based incompatibility that
is not present in oviparous species (Zeh & Zeh 1996,
1997, 2000, 2001). With viviparity, conflict can arise not
only between male and female mates, but also between
mothers and developing embryos and between sibling
embryos (see Spencer et al. 1998, 1999). Second, as this
study demonstrates, the ability of viviparous females to
engage in trading up from an unpropitious first partner
may be constrained by detrimental effects of abortion on
sexual receptivity that obviously are not experienced by
females that lay eggs. For a viviparous female, mating
with more than one male before attempting to reproduce
would seem to have two advantages over the trading-up
strategy. A multimale sperm pool not only minimizes the
multiply mating smooth newts: females become more choosy.
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a mixed-paternity brood, thereby allowing females to
shunt maternal resources from any failing, defective
embryos to embryos that are developmentally viable. At
least in the case of C. scorpioides, it seems likely that
pre-emptive polyandry rather than facultative polyandry
provides these viviparous females with the best defence
against the negative impact that complete brood abortion
can have on their future reproductive success.
Acknowledgments
We thank the Instituto Nacional de Recursos Naturales
Renovables for permission to collect pseudoscorpions in
the Republic of Panama, the Smithsonian Tropical
Research Institute for logistical support and Tim Birk-
head, Scott Newcomer, Patty Gowaty and an anonymous
referee for comments on the manuscript. The research
was supported by the National Geographic Society, and
by grants from the National Science Foundation to J.A.Z
(IBN-9603735) and D.W.Z. (IBN-9514245).
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433ZEH & ZEH: CONSTRAINTS ON FACULTATIVE POLYANDRY