Behavioral Ecology Vol. 13 No. 2: 209-215
© 2002 International Society for Behavioral Ecology
High frequency of polyandry in a lek mating system
a Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada b Department of Zoology, University of Leicester, Leicester LE1 7RH, UK c Department of Biology, University of Oulu, PO Box 3000, Oulu, FIN-90014, Finland
Address correspondence to D.B. Lank. E-mail: dlank{at}sfu.ca . O. Hanotte is now at the International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya. A. Ohtonen is now at the North Karellia Regional Environment Centre, P.O. Box 69, FIN-80101 Joensuu, Finland. T. Burke is now at the Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Received 6 November 2000; revised 3 April 2001; accepted 18 May 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The adaptive significance of polyandry by female birds in the absence of direct benefits remains unclear. We determined the frequencies of polyandrous mating and multiple paternity in the ruff, a lekking shorebird with a genetic dimorphism in male mating behavior. More than half of female ruffs mate with, and have clutches fertilized by, more than one male. Individual females mate with males of both behavioral morphs more often than expected. Polyandrous mating was more likely following copulation interference, but interference was uncommon. The multiple paternity rate of ruffs is the highest known for avian lekking species and for shorebirds. The general hypothesis that pair-bond constraints are the major selective factor favoring multiple mating in birds does not predict our findings. Active genetic diversification, which has been widely dismissed as a functional explanation for polyandrous mating in birds, may apply with respect to the behavioral polymorphism in ruffs because of a Mendelian genetic basis for male behavioral morph determination and aspects of male—male cooperation and female choice. However, rates of multiple paternity in other species of lekking birds are higher than generally realized, and the potential benefits of diversification in general deserve further consideration.
Key words: alternative mating behavior, female choice, leks, multiple paternity, Philomachus pugnax, polyandry, ruffs, sperm competition.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Females often copulate with several males during a breeding attempt, but the adaptive significance of polyandry, if any (Halliday and Arnold, 1987
),
often appears enigmatic (Birkhead and
Møller, 1992; Jennions
and Petrie, 2000; Petrie and
Kempenaers, 1998; Westneat et
al., 1990; Yasui,
1998). Female birds clearly benefit when polyandry increases their
access to resources or paternal care provided by males, or their likelihood of
obtaining future mates (e.g., Galapagos hawks, Buteo galapagoensis:
Faaborg et al., 1980;
dunnocks, Prunella modularis:
Hatchwell and Davies, 1990;
spotted sandpipers, Actitis macularia:
Colwell and Oring, 1988;
Lank et al., 1985).
Polyandrous mating appears to increase offspring fitness in several groups of
animals (e.g., adders, Vipera berus:
Madsen et al., 1992; guppies,
Poecilia reticulata: Evans and
Magurran, 2000; bumble bees, Bombus terrestris:
Baer and Schmid-Hempel, 1999),
but the mechanisms producing the increases are unclear
(Jennions and Petrie,
2000).
In pair-bonded species, including many birds, certain females may attempt
to improve the genetic content of their offspring through extrapair
copulations, despite potential retaliation from their social mates
(Birkhead and Møller,
1992; Westneat et al.,
1990). Many published studies of birds document nonrandom choice
of extrapair mates, or second mates in non—pair-bonded species, which
suggests choice for particular phenotypes potentially related to good genes
(Birkhead, 1998;
Jennions and Petrie, 2000).
There are exceptions to this pattern, however, and experimental demonstrations
are few (see Hillgarth, 1990).
One alternative hypothesis is that genetic diversification of offspring per se
is favored. Although genetic diversification is a universal consequence of
polyandry, it has widely been assumed to be inapplicable for birds in general
(Westneat et al., 1990).
In lekking species, females choose mates without risking the loss of
support from males, which provide no support to begin with. In the absence of
this cost, if polyandry is advantageous, we would expect to find higher rates
of polyandry among lekking than among pair-bonded species. Alternatively,
because many females may readily mate with the best male at a lek, there may
be no benefit from copulating with several males, in contrast to the
pair-bonded situation. In many species of lekking grouse, females do have low
rates of copulation and are overwhelmingly monogamous
(Alatalo et al., 1996), as
predicted by this latter logic. This was previously assumed to be a general
pattern for lekking birds (Birkhead,
1998; Birkhead and
Møller, 1992; Birkhead
et al., 1987; Höglund and
Alatalo, 1995). However, females in some lekking species of other
groups of birds were more likely to be polyandrous when their mate choice was
constrained by interference from males
(Trail, 1985) or if males were
temporarily monopolized by other females
(Petrie et al., 1992).
Polyandry in lekking species may also occur if assessment criteria are subject
to error (Yasui, 1998), and in
less well-understood situations (see
Lanctot et al., 1997).
The ruff (Philomachus pugnax) is a lekking species in which
females mate relatively frequently (Petrie
and Kempenaers, 1998). The ruff is also unique among all birds in
having a genetic dimorphism in male mating behavior. Two male morphs differ in
both plumage and behavior, with darker plumaged, "independent"
males defending adjacent small mating courts (ca. 1-1.5m2), and
lighter plumaged, nonterritorial "satellite" males displaying with
independents on the independents' courts
(Hogan-Warburg, 1966;
van Rhijn, 1991). The morph
ratio is about 84% independents to 16% satellites over the entire breeding
range from northern Europe to eastern Siberia (van Rhijn,
1983,
1991;
Widemo, 1998). Genetically,
independent males are homozygous recessive at the behavior locus, and 90% of
satellites are heterozygotes (Lank et al.,
1995).
In this article, we describe the mating patterns of wild female ruffs, called "reeves," with respect to male interference and male morph. We examined the rates of multiple paternity of clutches using DNA markers. We discuss our findings with respect to proximate and ultimate hypotheses regarding the causes and significance of polyandry in female birds.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
We studied reeves mating along the south and east shoreline of Liminganlahti (ca. 60°50' N, 25°20' E), about 30 km south-southwest of Oulu, Finland, during May and June of 1984-1987 and 1989-1990. We made daily observations throughout these breeding seasons from blinds located 15-30 m from leks, observing birds with binoculars and through 20-60xspotting scopes (Lank and Smith, 1987
).
We recorded the mating behavior of females. A lek visit began when a reeve
arrived and ended when she left. We tabulated mating behavior, including
female crouches (Hogan-Warburg,
1966; Shepard,
1975), attempted copulations by males, apparently successful
copulations, and copulation interference by other males. We scored a
"mating attempt" when a female crouched, and a
"mating" when a male mounted her. We tallied a "mating
visit" when a female mated one or more times. "Multiple
mating" means copulating more than once, with one or more male(s). We
tallied the number of independent and satellite males present during each
mating visit.
We used data from individually identifiable reeves to examine the timing of
lek visitation relative to egg laying, mating behavior between successive
visits, and mating behavior over an entire nesting attempt and season. Most
identifiable reeves (83%) were captured and color-banded in years before the
lek visits reported here, but we also include data from 10 unbanded females
with extremely distinctive plumage characteristics. Because individual reeves
may mate at several locations (including off the lek;
Lank and Smith, 1987), matings
occur throughout the long arctic days, and our observation schedules differed
within and among years, our mating histories are incomplete, and our direct
tallies of polyandrous mating rates are thus minimal.
Nearby males may interfere with mating attempts. Neighbors may threaten from their courts or charge, and neighbors and court co-occupants of either morph may attack a copulating pair. We scored mating interference only when there was physical contact and tallied the morph of the interfering male.
We searched intensively for nests in suitable habitat within approximately
2 km of lek sites, starting about a week after the first peak of mating. We
found nests that survived to hatch laid by 13 out of 61 reeves identified at
leks. We used the hatch dates from these nests, plus egg-laying and incubation
periods determined for wild and captive birds, to estimate the time of lek
visits and mating relative to egg-laying (wild: 5-7 days to lay 4 eggs and 22
days to hatch: Andersen, 1944;
Kondrat'yev, 1982; captivity:
5-6 and 22.3 days: Lank and Smith, unpublished data).
In 1987, 1989, and 1990, we collected blood samples from 9, 25, and 15 males, respectively, at leks under observation, from females trapped on nests ranging from 20 to 1500 m from the leks, and from offspring from these nests. In 1987, blood samples were taken from newly hatched chicks in the field. In 1989 and 1990, we collected clutches, incubated the eggs, and took blood samples from hatching young. DNA isolated from embryos of a few unhatched eggs was also used. Although all broods considered in this analysis initially had 4 eggs, we obtained DNA data from a mean of 3.0 chicks per brood (range 2-4).
We analyzed DNA extracted from samples using one of two techniques. The
1987 samples (n = 4 broods) were probed with multilocus DNA probes
(Jeffreys 33.15 and 33.6; Bruford et al.,
1998; Jeffreys et al.,
1985), and the 1989 and 1990 samples (n = 30 broods) were
analyzed using five single-locus minisatellite probes developed from the ruff
genome (Hanotte, Bailey, and Burke, unpublished data;
Lank et al., 1995). We
categorized each brood as having single versus multiple paternity using one of
three criteria: (1) a single father was identified for all chicks in a brood,
or more than one father was assigned; (2) for the single-locus analyses only,
if no father was identified for broods of three or more offspring, single
paternity was scored if the offspring shared not more than two nonmaternal
allele(s) for each of the five probes tested, whereas multiple paternity was
scored if three or more different paternal alleles occurred at two or more
loci; (3) for the single-locus analyses only, if no father was identified for
broods of two offspring, multiple paternity was scored if the brood did not
share paternal alleles at any of the five loci. Using these criteria, the
probability of misclassification as multiple paternity is, for case 2,
estimated as 10-5, found from binomial expectation based
conservatively on an expected mean mutation rate for minisatellite loci of
10-3 (Jeffreys et al.,
1988) and, in case 3, equal to the probability that a heterozygote
father for all five probes will transmit a different allele to each offspring
for all five probes (p =.03 or less because two fathers could share
alleles at some loci). These criteria are conservative and will underestimate
the rate of multiple paternity. For offspring of known fathers
(Lank et al., 1995), we
tallied paternity by morph.
We determined the proportion of independent and satellite males in our
local area by surveying ruffs throughout one of our study sites daily in 1986
and 1987 (Lank and Smith,
1987) and assigning a behavioral morph to each male based on his
behavior or plumage coloration
(Hogan-Warburg, 1966).
Surveying decreased potential biases in morph ratio estimates based only on
data from leks (see Widemo,
1998).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Mating patterns
Individually identified reeves visited leks between 25 and 34 days before their eggs hatched (Figure 1). Allowing 5 days for laying and 22 for incubation (see Methods), reeves visited the lek for about 1 week before laying their first egg. Females mated on about 1 lek visit in 10 (Lank and Smith, unpublished data), concentrated 1-4 days before the start of laying. Although identifiable reeves nested as close as 20 m to a lek, we never saw visits during incubation.
|
During single mating visits, 37% of reeves mated multiply (Table 1). Among these, 24% mated polyandrously, including three trigamous reeves. The mean number of matings per visit did not differ between multiply mating monogamous and polyandrous females (Table 1; t = 0.31, df = 103, p =.76). Thus, polyandry within visits did not occur simply because certain multiply mating females copulated more often than others.
|
Among identifiable females with two or more mating visits, six of nine were polyandrous (Table 1); one of these was also polyandrous within a visit. Seven additional females attempted to mate on two or more visits, but failed on one or both. Six of these seven would have been polyandrous had they mated on both visits. Thus, 12 of 16 females attempted to be polyandrous between visits. Four of the six successfully polyandrous females clearly switched mates, since both chosen males were present on both mating visits. One female mated with two different satellites, each of which was present on only one visit. The sixth female mated with independent males on two leks approximately 1.4 km apart. Finally, we observed four additional females mating before laying two separate clutches. One changed mates, two remated with their original male, and one remated with her original male but also mated with a second male. Although these samples are small, they suggest that a majority of females change males within or between clutches.
Mating histories of individuals
We compiled lek visit histories for 61 individually identifiable reeves. We
observed 1-13 visits over 1-7 days before single nesting attempts
(Table 2). We saw no mating
attempts for 27 of these females. Assuming that these females did mate at
least once, we missed about half or more of the matings at our sites. The
females we observed attempting to mate did so 3.3 times, on average, ranging
up to 13. Seventy-four percent of this group (25/34) made more than one mating
attempt, and 38% did so with more than one male. Thus, among all females we
observed crouching or mating more than once, 52% (13/25) did so with more than
one male. Two females attempted to mate with five different males. There was
no significant difference between the mean number of lek visits or number of
mountings by males for multiply mating monogamous and polyandrous females
(visits: 4.0 vs. 5.0, t = 0.79, df = 23, p =.45; matings:
1.9 vs. 2.8, t = 0.81, df = 17.3, p =.43). However, the
number of mating attempts by females may have been higher for polyandrous
females (3.0 vs. 5.2, t = 2.04, df = 14.6, p =.06).
|
Mating interference
Intruding males or court co-occupants interfered with matings during 11.3%
of the 612 copulation attempts we observed. To compare rates of male
interference during multiply mating monogamous versus polyandrous mating
visits, we classified visits as interfered with only if the interference
occurred before a mate switch or before the last mating attempt during that
visit. Interference was more frequent for females subsequently mating
polyandrously than for monogamous females who mated multiple times (7/72 for
monogamous visits versus 8/23 for polyandrous visits; 
2 =
8.23, df = 1, p =.004). In half (4/8) of the polyandrous cases, the
female subsequently mated with the interfering male. Interference occurred at
a similar rate during mixed-morph polyandrous mating visits (6/14) as those
with independents only (2/9; Fisher's Exact test, p =.38).
Multiple paternity rates
We determined single versus multiple paternity for 34 broods
(Table 3). Exactly half had
multiple paternity, including three with three fathers. The average brood thus
had at least 1.6 fathers. Similar results were obtained in all 3 years and
with both paternity assessment techniques. We did not detect a higher
frequency of multiple paternity when more samples per brood were obtained.
Nonetheless, the true multiple paternity rate is likely to be higher than 50%
because we obtained data for only 3.0 of the 4 chicks per brood, on average.
With data from two of four chicks, we have a 50% chance of having missed
multiple paternity had it occurred, and we had a 30% chance of missing
additional fathers from three chick broods. If we conservatively assume a mean
of 1.6 fathers per brood, based on our incomplete sample, we expect that 3 of
the 12 single-paternity clutches with incomplete information in
Table 3 were multiply sired.
Thus we estimate a multiple paternity rate of 59%.
|
Female mating behavior with respect to male morph
Reeves mating with independent males were more likely to mate multiply
during a mating visit than those mating with satellites
(Table 4; 2 =
8.11, df = 1, p =.004). Among multiply mating females, those mating
with independents copulated more often per mating visit than those mating with
satellites (3.0 vs. 2.2, t = 3.55, df = 41.2, p =.001).
|
Polyandrous females mated nonrandomly with respect to male morph type. On surveys, we found the proportion of independent males to be 0.840 ± 0.006 in 1986 (n = 24 days) and 0.838 ± 0.006 in 1987 (n = 16 days), for an overall mean of 0.839. If reeves change mates randomly with respect to male morph, the binomial expectation is 0.70 independent male combinations, 0.27 both morphs, and 0.03 both satellites. Out of 23 reeves observed to mate polyandrously, 14 mated with both morphs, twice as many as expected (Table 5). In nine of these cases, females mated first with an independent, and in five cases first with a satellite.
|
Because the proportion of independent males at leks may differ from that in the general population, we calculated the proportion at the lek when a female mated with the second male. The morph ratio when independent—independent combinations occurred was 0.76 independents, and when independent—satellite switches occurred was 0.82, suggesting a slight overrepresentation of satellites at leks relative to our censuses. The two ratios did not differ significantly, so we used the weighted mean of 0.80 as an expected value. Females still mated with both morphs significantly more often than expected by chance (Table 5).
We also looked at the mate choices of females seen to change mates between visits before laying a single clutch (Table 5). Two of six switched morphs. If we tally mating attempts rather than matings, seven of 12 polyandrous females attempted to mate only with independents, four attempted to mate with both morphs, and one attempted to mate with two satellites and no independents. The four females seen mating during two nesting attempts all remated with the same morph. One mated with the same independent male and one with the same satellite, one changed from one independent male to another, and one mated with the same independent male for both clutches but also mated with a second independent male on her second clutch.
We assessed the paternal morph ratios of clutches with known fathers. Two single-paternity broods were fathered by an independent and two by a satellite father. Three multiple-paternity broods were fathered by an independent and a male of unknown morph; one was fathered by two independent males and a third male of unknown morph; two were fathered by an independent, a satellite male, and a male of unknown morph; one was fathered by a satellite and a male of unknown morph; and three were fathered by two satellite males.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Most female ruffs are polyandrous
Half of the clutches analyzed demonstrated multiple paternity, and given our less than complete information (Table 3) and conservative assignment criteria (see Methods), we estimate 59% as a minimum estimate of the true rate of multiple paternity. It is difficult to quantitatively compare behavioral and genetic rates of polyandry because our behavioral data are substantially incomplete. However, just more than half of the individually recognizable females we saw attempting to mate more than once did so with more than one male (Table 2). Because only 8% of females mated polyandrously during single lek visits (Table 1), the preponderance of multiple paternity must be due to mate changes between mating visits, as occurred in six of the nine cases of mating during two visits that we did observe (Table 1).
If the probability that a female will mate with a new male is independent
between mating visits and independent of her status as polyandrous or not
within visits, females with one to four mating visits would have had polyandry
rates of 8%, 70%, 90%, and 97%, respectively. Van Rhijn
(1983) reported that a few
distinctively plumaged reeves each mated on about three different visits.
We conclude that the majority of reeves are both behaviorally and
genetically polyandrous. These are the highest rates estimated for any lekking
bird species (Lanctot et al.,
1997; Wiley, 1991)
and also the highest for any shorebird species (see references in
Johnson and Briskie, 1999; see
also semipalmated plover, Charadrius semipalmatus, 4%:
Zharikov and Nol, 2000; ringed
plover, Ch. hiaticula, 0%:
Wallander et al., 2001; great
snipe, Gallinago media, 2/7 families: Bailey, Kålås JA,
and Burke, unpublished data; Wilson's phalarope, Phalaropus
tricolour, 0%: Delehanty et al.,
1998; red-necked phalarope, P. lobatus, 6%:
Schamel, 2000; western
sandpiper, Calidris mauri, 5%:
Blomqvist et al., in
press).
Females fertilized eggs using stored sperm
(Figure 1), and the sperm size
of ruffs supports an evolutionary history of sperm competition and multiple
paternity. In passerine birds (Briskie et
al., 1997) and shorebirds
(Johnson and Briskie, 1999),
sperm size increases with higher rates of multiple paternity, and ruffs have
the longest sperm of any shorebird yet measured
(Johnson and Briskie, 1999;
Lank et al., unpublished data).
Is female choice constrained by male interference?
Courtship interference occurred on 11% of mating attempts, similar to rates
in Götland, Sweden (Widemo,
1997,
1998). This rate is low
compared to that of multiple paternity, and mate changes between visits
account for most of our estimated multiple-paternity rate. Thus, interference
is not a proximal cause of most of the multiple paternity in ruffs.
Nonetheless, a third of the polyandrous matings we observed during single lek
visits were preceded by physical interference with a copulation attempt before
the female mated with a second male, and multiply-mating reeves were more
likely to be polyandrous after male—male interference, as also occurs in
black grouse (Tetrao tetrix;
Alatalo et al., 1996). This
does not necessarily mean that female choice is substantially constrained by
male interference (Sæther et al.,
1999), but females may use interference in making mate-choice
decisions (Avery, 1984).
Females subsequently mated with interfering males in four of eight cases we
observed. Such redirected mate choice has been reported for Guianan
cock-of-the-rock Rupicola rupicola
(Trail, 1985;
Trail and Koutnik, 1986), but
not in other lekking species in which interference was reported (e.g.,
Alatalo et al., 1996),
including two lekking shorebirds (great snipe:
Sæther et al., 1999;
buff-breasted sandpiper, Tryngites subruficollis:
Lanctot et al., 1997).
Do female ruffs actively genetically diversify their offspring?
Why is polyandry unusually frequent in ruffs relative to other lekking
species and to related shorebirds? Several hypotheses seem inapplicable in
this case. Neither good genes nor better genes
(Birkhead, 1998;
Jennions and Petrie, 2000),
nor fertility insurance (Sheldon,
1994), nor inducing direct sperm competition and/or sperm
selection by females (Yasui,
1997; but see Curtsinger,
1991) predict disproportionate crossmorph mating
(Table 5). This intriguing
observation is instead consistent with the hypothesis that females actively
diversify their offspring with respect to male morph.
Increased genetic diversification of offspring is a universal result of
polyandrous mating by females, but it has been consistently dismissed as an
unlikely ultimate explanation for polyandrous mating by female birds in
general (e.g., Birkhead and Møller,
1992; Westneat et al.,
1990; Williams,
1975; Yasui, 1998)
and in specific cases (e.g., Ligon and
Zwartjes, 1995; Petrie et al.,
1992; Wagner et al.,
1996; Westneat,
1992, and many authors do not even discuss the possibility (e.g.,
Kempenaers et al., 1992;
Sheldon, 1994; but see
Dunn et al., 1994;
Strohbach et al., 1998;
Taylor et al., 2000, for
possible cases). Three common objections against its importance
(Westneat et al., 1990) may be
less applicable for the specific trait of male behavioral morph. First,
females will substantially increase the genetic diversity of their offspring
through multiple mating, at least with respect to male morph. Male morph is a
Mendelian rather than quantitative trait, with autosomal inheritance and a
dominant satellite allele (Lank et al.,
1995,
1999). Females can
theoretically allocate their genetic and behavioral "male morph
investment" only by mating with both morphs. Because 86% of females are
homozygous recessive at the morph locus, they will produce only independents
if they mate with independents, and approximately equal proportions of
satellite and residents by mating only with a satellite. Second, a theoretical
decrease in parental fitness through increased sib competition in mixed broods
(Sherman, 1981) is less
applicable in a precocial species with a small clutch size. Finally, because
most reeves do pursue polyandrous matings, rather than only females whose
partners are perceived as being of lower genetic quality
(Birkhead, 1998;
Jennions and Petrie, 2000;
Westneat et al., 1990), an
adaptive role for diversification per se is plausible.
What benefits might females obtain from diversification? The most
intriguing theoretical possibility is half-sib cooperation among offspring
(Yasui, 1998). Combinations of
independent and satellite males apparently attract females to courts
(van Rhijn, 1973;
Widemo, 1998), thereby
stabilizing the maintenance of the male dimorphism
(Hugie and Lank, 1997).
Co-display by independent and satellite brothers would decrease the fitness
costs of sharing matings with a co-occupant. Although satellites track female
movements among leks (Lank and Smith,
1987; van Rhijn,
1983,
1991) and among males within
leks (Widemo, 1998), they also
form temporary associations with particular independents
(van Rhijn, 1991). If the
frequency and payoff for half-sib associations were sufficiently high, this
mechanism could offset a female's costs of pursuing polyandrous matings
between morphs. Although the exceptionally cooperative males at long-tailed
manakin display sites are unrelated
(McDonald and Potts, 1994),
genetic structure does exist among leks of black grouse
(Höglund et al., 1999)
and white-bearded manakins (Manacus manacus;
Shorey et al., 2000), and
kin-biased association at display sites was found among feral peacocks
(Pavo cristatus) raised experimentally in non-sib groups
(Petrie et al., 1999).
Polyandry in lekking species
Lekking species have been characterized as having low rates of multiple
mating and multiple paternity (Birkhead,
1998; Birkhead and
Møller, 1992; Birkhead
et al., 1987), based primarily on the low mating rates of lekking
grouse (Alatalo et al., 1996;
Höglund and Alatalo,
1995; Wiley, 1991)
and supported by the logic that multiple mating was unnecessary because highly
attractive males were readily available to all females
(Westneat et al., 1990).
However, multiple paternity in several lekking species is more frequent than
expected from this point of view. In white-bearded manakins, buff-breasted
sandpipers, peafowl, the Guianan cock-of-the-rock, and ruffs, a quarter or
more of females mated with more than one male (see
Lanctot et al., 1997). Because
females of lekking species do not face the potential cost of loss of male
support, and search costs are low, the costs of polyandry may also be low.
Given low costs, any of the many potential genetic benefits from polyandry
(Jennions and Petrie, 2000),
including sperm competition and/or sperm selection by females
(Yasui, 1997) or more exotic
direct benefits (e.g., Lombardo et al.,
1999) may result in its spread. Höglund and Alatalo
(1995) suggested that the most
likely factor selecting against polyandrous mating in lekking species was
avoidance of disease. Strongly skewed mating systems have tremendous potential
for spreading sexually transmitted diseases
(Hamilton, 1990;
Lombardo, 1998), and polyandry
may pay with respect to the coevolution of disease resistance
(Møller, 1997). For
whatever reason, a female's mating rule in many lekking species may be not the
oft-stated search for the highest quality male, but rather to seek several
high quality mates.
|
ACKNOWLEDGEMENTS |
|---|
For assistance in the field and with aviculture, we thank J. Reynolds, J. Maron, T. Muotka, M. Sirvio, M. Koskinen, K. Lessells, C. Francis, L. Hogan-Warburg, A. Muldal, S. Savage, D. McRae, J. Mountjoy, P. Nieminen, J. Pönne, J. Roosma, A. I. Brown, L. Kuehner, I. Anttila, and T. Liukkonen. The research was facilitated by generous support from colleagues at the University of Oulu, including R. Strömmer and E. Pulliainen, and from F. Cooke. We thank D. Blomqvist for permission to cite unpublished data and communal landowners of the Liminganlahti shoreline for permission to work these areas. This research was supported by grants to D.B.L. from the National Science Foundation, the Natural Sciences and Engineering Research Council (NSERC), the H.F. Guggenheim Foundation, the National Geographic Society, and the Fulbright Program; by NSERC grants to F. Cooke, and by Natural Environment Research Council grants to T. Burke.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alatalo RV, Burke T, Dann J, Hanotte O, Höglund J, Lundberg A, Moss R, Rintamäki PT, 1996. Paternity, copulation disturbance and female choice in lekking black grouse. Anim Behav 52: 861-873.
Andersen FS, 1944. Contributions to the breeding biology of the ruff (Philomachus pugnax). Dansk Ornithol Foren Tidssk 38: 26-30.
Avery MI, 1984. Lekking in birds: choice, competition and reproductive constraints. Ibis 126: 177-187.
Baer B, Schmid-Hempel P, 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumblebee. Nature 397: 151-154.
Birkhead TR, 1998. Sperm competition in birds: mechanism and function. In: Sperm competition and sexual selection (Birkhead TR, Møller AP, eds). San Diego, California: Academic Press; 579-622.
Birkhead TR, Atkin L, Møller AP, 1987. Copulation behaviour of birds. Behaviour 101: 101-138.[ISI]
Birkhead TR, Møller AP, 1992. Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
Blomqvist D, Kempenaers B, Lanctot RB, Sandercock BK, in press. Genetic parentage and mate guarding in the arctic breeding western sandpiper. Auk.
Briskie JV, Montgomerie R, Birkhead TR, 1997. The evolution of sperm size in birds. Evolution 51: 937-945.[ISI]
Bruford MW, Hanotte O, Brookfield JFY, Burke T, 1998. Multilocus and single-locus DNA fingerprinting. In: Molecular genetic analysis of populations: a practical approach (Hoelzel AR, ed). Oxford: IRL Press; 225-269.
Colwell MA, Oring LW, 1988. Extra-pair mating in the spotted sandpiper: a female mate acquisition tactic. Anim Behav 38: 675-684.
Curtsinger JW, 1991. Sperm competition and the evolution of multiple mating. Am Nat 138: 93-102.
Delehanty DJ, Fleischer RC, Colwell MA, Oring LW, 1998. Sex-role reversal and the absence of extra-pair paternity in Wilson's phalaropes. Anim Behav 55: 995-1002.[ISI][Medline]
Dunn PO, Robertson R, Michaud-Freeman D, Boag, PT, 1994. Extrapair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35: 273-281.
Evans JP, Magurran AE, 2000. Multiple benefits of
multiple mating in guppies. Proc Natl Acad Sci USA
97: 10074-10076.
Faaborg J, de Vries T, Patterson CB, Griffin CR, 1980. Preliminary observations on the occurrence and evolution of polyandry in the Galapagos hawk (Buteo galapagoensis). Auk 97: 581-590.
Halliday T, Arnold SJ, 1987. Multiple mating by females: a perspective from quantitative genetics. Anim Behav 35: 939-941.
Hamilton WD, 1990. Mate choice near or far. Am Zool 30: 341-352.
Hatchwell BJ, Davies NB, 1990. Provisioning of nestlings by dunnocks, Prunella modularis, in pairs and trios: compensation reactions by males and females. Behav Ecol Sociobiol 27: 199-209.
Hillgarth N, 1990. Parasites and female choice in the ring-necked pheasant. Am Zool 30: 227-233.
Hogan-Warburg AL, 1966. Social behavior of the ruff, Philomachus pugnax (L.). Ardea 54: 109-229.[ISI]
Höglund J, Alatalo R, 1995. Leks. Princeton: Princeton University Press.
Höglund J, Alatalo RV, Lundberg A, Rintamaki PK, Lindell J, 1999. Microsatellite markers reveal the potential for kin selection on black grouse leks. Proc R Soc Lond B. 266: 813-816
Hugie DM, Lank DB, 1997. The resident's dilemma: a
female-choice model for the evolution of alternative male reproductive
strategies in lekking male ruffs (Philomachus pugnax). Behav
Ecol 8:
218-225.
Jeffreys AJ, Royle NJ, Wilson V, Wong Z, 1988. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable human DNA. Nature 332: 278-281.[Medline]
Jeffreys AJ, Wilson V, Thein SL, 1985. Hypervariable `minisatellite' regions in human DNA. Nature 314: 67-73.[Medline]
Jennions MD, Petrie M, 2000. Why do females mate multiply? A review of the genetic benefits. Biol Rev 75: 21-64.[Medline]
Johnson DDP, Briskie JV, 1999. Sperm competition and sperm length in shorebirds. Condor 101: 848-854.
Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broeckhoven C, Dhont AA, 1992. Extra-pair paternity results from female preference for high-quality mates in the blue tit. Nature 357: 494-496.
Kondrat'yev AY, 1982. The biology of waders on tundras of northeastern Asia. Moscow: Nauka Publishing House.
Lanctot RB, Scribner KT, Kempenaers B, Weatherhead PJ, 1997. Lekking without a paradox in the buff-breasted sandpiper. Am Nat 149: 1051-1070.[ISI]
Lank DB, Coupe M, Wynne-Edwards KE, 1999. Testosterone-induced male traits in female ruffs (Philomachus pugnax): autosomal inheritance and gender differentiation. Proc R Soc Lond B 266: 2323-2330.
Lank DB, Oring LW, Maxson SJ, 1985. Mate and nutrient limitation of egg-laying in a polyandrous shorebird. Ecology 66: 1513-1524.
Lank DB, Smith CM, 1987. Conditional lekking in ruff (Philomachus pugnax). Behav Ecol Sociobiol 20: 137-145.
Lank DB, Smith CM, Hanotte O, Burke TA, Cooke F, 1995. Genetic polymorphism for alternative mating behavior in lekking male ruff, Philomachus pugnax. Nature 378: 59-62.
Ligon JD, Zwartjes PW, 1995. Female red junglefowl choose to mate with multiple mates. Anim Behav 49: 127-135.
Lombardo MP, 1998. On the evolution of sexually transmitted diseases in birds. J Avian Biol 29: 314-321.
Lombardo MP, Thorpe PA, Power HA, 1999. The beneficial
sexually transmitted microbe hypothesis of avian copulation. Behav
Ecol 10:
333-337.
Madsen T, Shine R, Loman J, Håkansson T, 1992. Why do female adders copulate so frequently? Nature 355: 440-441.
McDonald DB, Potts WK, 1994. Cooperative display and
relatedness among males in a lek-mating bird. Science
266: 1030-1032.
Møller AP, 1997. Immune defense, extra-pair paternity, and sexual selection. Proc R Soc Lond B 264: 561-566.
Petrie M, Hall M, Halliday T, Budgey H, Pierpoint C, 1992. Multiple mating in a lekking bird: why do peahens mate with more than one male and with the same male more than once? Behav Ecol Sociobiol 31: 349-358.
Petrie M, Kempenaers B, 1998. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13: 52-58.
Petrie M, Krupa A, Burke T, 1999. Peacocks lek with relatives even in the absence of social and environmental cues. Nature 401: 155-157.
Sæther SA, Fiske P, Kålås JA, 1999. Pushy males and choosy females: courtship disruption and mate choice in the lekking great snipe. Proc R Soc Lond B 266: 1225-1234.
Schamel DL, 2000. Male and female mating strategies in red-necked phalarope (PhD dissertation). Burnaby, British Columbia: Simon Fraser University.
Sheldon BC, 1994. Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257: 25-30.
Shepard JM, 1975. Factors influencing female choice in the lek mating system of the ruff. Living Bird 14: 87-111.
Sherman PW, 1981. Electrophoresis and avian genealogical analysis. Auk 98: 419-422.
Shorey L, Piertney S, Stone J, Höglund J, 2000. Fine-scale genetic structuring on Manacus manacus leks. Nature 408: 352-353.[Medline]
Strohbach S, Curio E, Bathen A, Epplen JT, Lubjuhn T,
1998. Extrapair paternity in the great tit (Parus
major): a test of the "good genes" hypothesis. Behav
Ecol 9:
388-396.
Taylor EL, Blache D, Groth D, Wetherall JD, Martin GB, 2000. Genetic evidence for mixed parentage in nest of the emu (Dromaius novaehollandiae). Behav Ecol Sociobiol 47: 359-364.
Trail PW, 1985. Courtship disruption modifies mate
choice in a lekbreeding bird. Science
227: 778-780.
Trail PW, Koutnik DL, 1986. Courtship disruption at the lek in the Guianan cock-of-the-rock. Ethology 73: 197-218.
van Rhijn JG, 1973. Behavioral dimorphism in male ruffs, Philomachus pugnax (L.). Behavior 47: 153-229.
van Rhijn JG, 1983. On the maintenance and origin of alternative strategies in the ruff Philomachus pugnax. Ibis 125: 482-498.
van Rhijn JG, 1991. The ruff: individuality in a gregarious wading bird. London: Academic Press.
Wagner RH, Schug MD, Morton ES, 1996. Condition-dependent control of paternity by female purple martins: implications for coloniality. Behav Ecol Sociobiol 38: 379-389.
Wallander J, Blomqvist D, Lifjeld JT, 2001. Genetic and social monogamy—does it occur without mate guarding in the ringed plover? Ethology 107: 561-572.
Westneat DS, 1992. Do female red-winged blackbirds engage in a mixed mating strategy? Ethology 92: 7-28.[ISI]
Westneat DF, Sherman PW, Morton ML, 1990. The ecology and evolution of extra-pair copulation in birds. In: Current ornithology, 7th ed (Power DM, ed). New York: Plenum Press; 331-369.
Widemo F, 1997. The social implication of traditional
use of lek sites in the ruff, Philomachus pugnax. Behav
Ecol 8:
211-217.
Widemo F, 1998. Alternative reproductive strategies in the ruff, Philomachus pugnax: a mixed ESS? Anim Behav 56: 329-336.[ISI][Medline]
Wiley RH, 1991. Lekking in birds and mammals: behavioral and evolutionary issues. Adv Stud Behav 20: 201-291.
Williams GC, 1975. Sex and evolution. Princeton, New Jersey: Princeton University Press.
Yasui Y, 1997. A "good-sperm" model can explain the evolution of costly multiple mating by females. Am Nat 149: 573-584.[ISI]
Yasui Y, 1998. The "genetic benefits" of female multiple mating reconsidered. Trends Ecol Evol 13: 246-250.
Zharikov Y, Nol E, 2000. Copulation behavior, mate guarding, and paternity in the semipalmated plover. Condor 102: 231-235.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  R. Duraes, B. A. Loiselle, and J. G. Blake Intersexual spatial relationships in a lekking species: blue-crowned manakins and female hot spots Behav. Ecol., November 1, 2007; 18(6): 1029 - 1039. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. Tang-Martinez and T. B. Ryder The Problem with Paradigms: Bateman's Worldview as a Case Study Integr. Comp. Biol., November 1, 2005; 45(5): 821 - 830. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||