Behavioral Ecology Vol. 10 No. 5: 472-475
© 1999 International Society for Behavioral Ecology
Birth sex ratios relate to mare condition at conception in Kaimanawa horses
a Ecology Group, Institute of Natural Resources b Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11222, Palmerston North, New Zealand
Address correspondence to E. Cameron. E-mail. E.Z.Cameron{at}massey.ac.nz . C. J. Veltman is now at the Department of Conservation, Science and Research Division, PO Box 10420, Wellington, New Zealand.
Received 14 May 1998; revised 3 December 1998; accepted 18 January 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Several hypotheses have been proposed to explain variation in birth sex ratios, based on the premise that variation is expected when the profitability of raising sons and daughters varies between individual parents. We tested the Trivers-Willard hypothesis that mothers in better condition produce relatively more sons and that mothers in poorer condition produce relatively more daughters when male reproductive success is more variable. We examined birth sex ratios in relation to mare body condition at conception in horses in which male reproductive success is differentially helped by slight advantages in condition. Horses meet the assumptions of the Trivers-Willard hypothesis better than many species on which it has been tested and in which sex ratio biases are not confounded by sexual size dimorphism such that one sex is more likely to die in utero in females in poor condition. Mares that had a female foal were in poorer condition at conception than those that had a male foal, and mares that had foals of different sexes in different years were in significantly poorer condition when they conceived their female foal. There was no relationship between offspring sex and mid-gestation condition, and there was no difference in foaling rates in relation to body condition at conception. Consequently, sex ratio deviations are not explained by fetal loss in utero. Furthermore, differential fetal loss of the less viable sex cannot explain the greater proportion of males produced by mares in better condition. Therefore, our results suggest that sex ratio modification occurs at conception in wild horses.
Key words: birth sex ratios, Equus caballus, fetal loss, maternal condition, Trivers-Willard hypothesis, wild horses.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Sex ratios at birth and hatching can vary (Clutton-Brock, 1985
;
Clutton-Brock et al., 1986;
Clutton-Brock and Iason, 1986;
Frank, 1990;
Hardy, 1997). Adaptive
theories predict variation in birth sex ratio when the profitability of
raising sons and daughters varies between individual parents
(Trivers and Willard, 1973).
Large sex ratio variations were recently reported in Seychelles warbler eggs,
indicating differential conception of male and female offspring in relation to
offspring profitability (Komdeur et al.,
1997). In mammals, although variations in birth sex ratios tend to
be relatively small and some estimates have been based on inadequate evidence
(Festa-Bianchet, 1996), some
studies have shown significant variation
(Clutton-Brock and Iason,
1986).
The Trivers-Willard model suggests that where one sex has more variable
reproductive success, such as males in polygynous species, mothers in good
condition will be benefited by producing more of that sex, whereas mothers in
poor condition would be benefited by producing more of the reproductively
stable sex (Trivers and Willard,
1973). The hypothesis is appropriate for species with a small
litter size and depends on three premises
(Trivers and Willard, 1973):
(1) that the condition of the young at the end of parental investment will
tend to be correlated with the condition of the mother during parental
investment; (2) that these differences in condition tend to endure into
adulthood; and (3) that adult males will be differentially helped in
reproductive success by slight advantages in condition, such as through
intense male-male competition in polygynous species.
Wild horses meet these assumptions better than most mammal species on which
the hypothesis has been tested previously. Horse litter size is fixed at one
(Platt, 1978). Differential
investment in male and female offspring has been reported
(Berger, 1986;
Duncan et al., 1984), and this
varies with maternal condition: mares in good condition invest more in sons,
whereas mares in poor condition invest more in daughters (Cameron and
Linklater, submitted). There is a correlation between maternal rank (which is
related to condition, as dominant mares have access to better resources;
Duncan, 1992) and reproductive
success in both males (Feh,
1990) and females (Duncan,
1992), suggesting a correlation between female condition and
offspring condition and reproductive success as adults. However, because male
reproductive success is more variable, a mother's rank has a greater effect on
her son than on her daughter. In some other species, one sex may be easier to
invest in than the other. For example, where sons disperse and daughters are
philopatric, it may be easier to influence the reproductive success of
daughters for relatively little extra investment. This is not the case in
horses, where both male and female offspring disperse, and so there can be no
direct inheritance of social rank (Berger,
1986; Rutberg and Keiper,
1993). In addition, sexual size dimorphism at birth is minimal
(Duncan, 1992), so males are
not markedly more costly to raise in utero due to accelerated growth rates
alone, which has been a frequently cited reason that mothers in poor condition
lose more male offspring in other species
(Clutton-Brock, 1991).
Previous studies have examined offspring sex ratios in mammals in relation
to indices of condition such as food availability or diet (e.g.,
Monard et al., 1997;
Smith et al., 1996), maternal
ranking (e.g., Cassinello and Gomendio,
1996; Clutton-Brock et al.,
1984; Green and Rothstein,
1991), whether mothers were primiparous or multiparous (e.g.,
Cassinello and Gomendio, 1996),
reproductive success in the previous year (e.g.,
Green and Rothstein, 1991;
Rutberg, 1986), interval since
last offspring (e.g., Wiley and Clapham,
1993), or maternal body condition at slaughter when fetuses are
mature enough to be sexed (e.g., Reimars
and Lenvik, 1997; Wauters et
al., 1995). In Camargue horses, Monard et al.
(1997) found that sex ratios
were female biased in years following a season of poor food availability,
during which mares were in poorer body condition. However, they were unable to
determine if differences were due to differential conception or to
differential fetal loss during gestation. Estimates of female body condition
around (Kojola and Eloranta,
1989) or before (Moses et al.,
1995) conception provide more appropriate estimates at the time
when sex ratio adjustment can occur
(Krackow, 1995) than at times
that are more observable for researchers, but when adjustment does not
necessarily occur.
We aimed to determine if birth sex ratios vary according to the predictions of the Trivers-Willard hypothesis in relation to condition at conception both within and between individual mares. We examined differences in foaling rates of mares in different condition to determine if sex ratio variation is likely due to differential loss of offspring or to differences in conception sex ratio. Furthermore, we investigated variation in sex ratio in relation to the previously used indices of whether mares are primiparous or multiparous, previous year's foaling success, and mid-gestation condition.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Feral horses (Equus caballus), known locally as Kaimanawa horses, inhabit the Kaimanawa mountains and surrounding plateaus and valleys of central North Island, New Zealand. Since August 1994 we have been studying a population of approximately 400 of these horses which inhabit the Moawhango River basin and surrounding plateau. Individual horses were reliably identifiable by either freeze brands on their rumps or by natural markings.
Body condition scores were estimated by visual body fat distribution based
on an 11-point scale from 0-5 with 0.5 gradations
(Carroll and Huntingdon, 1988;
Huntingdon and Cleland, 1992;
Rudman and Keiper, 1991) with
the aid of 10-15x binoculars or a 15-60x telescope whenever horses
were sighted, provided visibility was good. Scores of 0 were very poor and
scores of 5 were obese. Interobserver reliability was high (r =.91).
In horses, body condition scores correlate with body fat percentage
(r =.81; Henneke et al.,
1983).
We calculated body condition at conception for Kaimanawa mares by
backdating from the date of foaling (accurate to ±5 days) by the
average gestation length±1 SD (336±10 days;
Kiltie, 1982) and taking the
mode of visual body condition scores during this period for foals born in
1995, 1996, and 1997, and at mid-gestation (168±10 days) for foals born
in 1995 and 1996. All mares used in the analysis were scored at least twice
during these 20-day periods, and mares were only scored once on any one day.
We also calculated modal body condition scores for mares in the month before
birth, and for foals in their 12th month to determine if female condition
during investment was reflected by foal condition near the end of the period
of investment.
Body condition scores at conception approximated a normal distribution, with the modal scores of most mares being 2.5 and a range of 1 to 4. Thirty-three mares foaled once, 30 foaled twice, and 14 foaled three times between 1994 and 1997.
We classified mares as primiparous if they had not foaled before and were
known to be too young (
2 years) to have foaled prior to the study
(n = 22). Mares were classified as multiparous only if they were
known to have foaled previously (n = 103; unknown, n = 10).
We also classified mares in relation to their previous year's reproductive
success (no foal or lost foal n = 67; successfully raised foal to 6
months, n = 67; unknown, n = 1).
We recorded the sex of every foal born to a mare within the focal population in the foaling season (September to February) starting in 1995 (n = 42), 1996 (n = 55), and 1997 (n = 38) by sighting genitalia, which are visible in both sexes from birth.
To determine if foaling rates were different between mares of different condition at conception, we recorded the condition of all mares during the mean conception date±1 SD (15 November-16 January 1994-95 and 1995-96) and recorded which of these mares foaled in the subsequent season.
The results of statistical tests presented are two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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There was a significant difference between the condition at conception of mares who had a female foal and mares who had a male foal (Mann-Whitney U test, U = 2794, N1 = 69, N2 = 66, p <.05). Mare condition at conception was a significant predictor of offspring sex (logistic regression,
2 = 7.89, df = 1, p <.01;
Figure 1). Furthermore, we
compared the condition at conception of mares that had foals of different
sexes and found that mares were in significantly poorer condition when they
conceived their female foal (Wilcoxon signed-ranks paired test, Z =
2.23, N = 25, p <.05).
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The sex ratio varied significantly from parity in both directions. Although differences were not significant for mares of condition 1, 1.5, 3, and 3.5, mares of condition 2 gave birth to significantly fewer sons than expected (binomial test, p <.01) and mares of condition 2.5 gave birth to significantly more sons than expected (binomial test, p <.05).
There was no difference in birth dates throughout the season for male or female offspring (Mean birth date = Mann-Whitney U test, U = 2205, N1 = 69, N2 = 66, ns). There was no significant variation in sex ratio between primiparous and multiparous mares, whether a mare had foaled in the previous year or in the year the foal was born in (Table 1).
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Although mare condition at conception was correlated with mare condition at
mid-gestation (rs =.36, n = 72, p
<.05), there was no difference in mare condition at mid-gestation between
mothers who had a male or female foal (Mann-Whitney U test,
U = 777, N1 = 41, N2 = 36,
ns), and mare condition at mid-gestation did not predict foal sex (logistic
regression, 2 = 0.31, df = 1, ns). The correlation was
stronger between condition at conception and condition during the month before
birth (rs =.64, n = 80, p <.001),
although mare condition before foal birth did not predict foal sex (logistic
regression, 2 = 1.11, df = 1, ns). There was also a
correlation between mare condition before birth and foal condition as
yearlings (rs =.62, n = 72, p
<.05).
There was no significant difference in foaling rates with condition at
conception (logistic regression, 2 = 0.34, df = 1, ns). About
30% of all mares did not foal.
In mares that foaled in subsequent years, there was a no difference in time between birth of the current foal and the conception of male or female foals (Mann-Whitney U test, U = 514, N1 = 37, N2 = 35, ns), though there was a tendency for males to be conceived after a longer period of time.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our study confirms the applicability of Kaimanawa horses as an ideal test of the Trivers-Willard hypothesis. Mares only ever had one foal per breeding attempt, and there was a correlation between mare body condition during investment and foal condition as yearlings when maternal investment was ending. Although we do not show that these advantages endure into adulthood, previous studies show increased reproductive success in the offspring of dominant mares (Duncan, 1992
;
Feh, 1990). Theoretically,
males will be differentially helped by condition advantages in a species as
highly polygnous as the horse.
Our results strongly support the predictions of the Trivers-Willard
hypothesis. In the Kaimanawa horse population, mares in poor condition at
conception gave birth to predominantly female foals, as did Camargue mares in
the year following a season of poor food availability
(Monard et al., 1997). There
was no significant difference in foaling rates in relation to condition at
conception, and about 30% of all mares did not produce a foal. Our 70% live
foal rate is similar to rates found in other studies of both domestic (50-80%;
Rossdale and Ricketts, 1980)
and wild (45-74%; Keiper,
1979; Keiper and Houpt,
1984) horses. Some unrecorded loss of neonates may also have
occurred, as neonatal mortality can be high in horses
(Berger, 1986;
Duncan, 1992;
Waring, 1983). However, live
foal rates were similar regardless of condition at conception, and death of
neonates is likely to be similar irrespective of the mother's earlier
condition. Therefore, it seems unlikely that the birth sex ratios we report
are due to differential death of fetuses or neonates by mares in poorer
condition. In addition, those mares who had a male foal in one year and a
female in another were in significantly poorer condition when they conceived
their female foal.
Furthermore, mares in better condition produced more male foals than
expected from an assumption of parity. Where sex ratios differ significantly
from parity in both directions, it is unlikely that the difference is due
solely to differential loss of less viable or more costly
fetuses—usually males in mammalian species
(Clutton-Brock, 1991). For sex
ratios that differ from parity in both directions to be explained by
differential loss of less viable or more costly fetuses, daughters would have
to be less viable in good-condition mares and sons less viable in
poor-condition mares (Clutton-Brock,
1991). Alternatively, mechanisms that favor the differential
conception of males or females have been postulated
(Krackow, 1995; e.g., timing
of insemination, Guerrero,
1974; Paul and Kuester,
1987; embryonic mortality,
Huck et al., 1988).
We found no difference in sex ratio between multiparous and primiparous
mares or whether a mare had foaled in the previous year. Furthermore, by
mid-gestation maternal condition was no longer a predictor of offspring sex
ratio, supporting the premise that sex ratios vary due to differential
conception of male and female offspring. Indeed, although condition during
gestation has been frequently used to examine sex ratio variation (e.g.,
supporting Trivers-Willard: Burke and
Birch, 1995; Kucera,
1991; Rutberg,
1986; Wauters et al.,
1995; not supporting Trivers-Willard:
Hewison and Gaillard, 1996;
Reimars and Lenvik, 1997),
such studies must assume that either sex ratios are adjusted during gestation
or that condition has not changed significantly since conception. In species
with long gestation, such as horses (11 months), condition may change
significantly during gestation. If males do cost more than females in utero,
as is suggested for several sexually dimorphic species
(Clutton-Brock, 1991), then
mothers carrying male offspring may lose more weight during pregnancy than
mothers carrying female offspring. Measures of body condition at or around
conception (e.g., Kojola and Eloranta,
1989; Moses et al.,
1995) provide a more accurate test of the Trivers-Willard
hypothesis than measures taken during gestation if, as our data suggest,
biases are caused by differential conception of males and females and not by
differential loss of fetuses during gestation.
Previous studies on mammals have documented variation in sex ratio in
relation to female weight around the time of conception, in line with the
prediction that females in good condition produce more male offspring
(reindeer: Kojola and Eloranta,
1989; bushy-tailed woodrats:
Moses et al., 1995),
suggesting differential conception may be occurring. In Kaimanawa horses, the
birth sex ratio differs from parity in both directions depending on mare
condition at conception, and variations in the birth sex ratio are too large
to be accounted for by differential fetal loss alone. In addition, there is no
variation in sex ratio in relation to condition during gestation. Therefore,
our data suggest that the sex ratio variation occurs near to conception and
before sexual differentiation.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This study was funded by New Zealand Department of Conservation contract no. 1850 to Massey University. Our thanks to the Army Training Group Waiouru (Operations Branch HQ ATG, Property Management Section, and Waiouru Support Company, 4th Logistics Battalion), who gave permission to work in the Army Training Area and provided some logistic support. The manuscript was greatly improved by comments from Ed Minot, Rachel Standish, Tarmo Põldmaa, and two anonymous reviewers.
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