Transcript Mating Systems IV: Leks B, Polyandry

Mating Systems IV:
Leks (Part B), Polyandry
Spotted sandpiper
JodyLee Estrada Duek, Ph.D.
With assistance from Dr. Gary Ritchison
http://people.eku.edu/ritchisong/matingsystems.html
The Lek Paradox 1
• Lekking males are
thought to face strong
directional selection on secondary sexual traits
• How variation in male traits can persist under these
conditions remains a problem: the lek paradox
• Over 200 papers have been published in the past
three decades on the lek paradox
• Because the costs of choice among lekking males
should be low, leks offer good systems for
addressing questions of female mate choice.
The Lek Paradox 2
• Studies show female choice for certain male traits on leks
(reviewed Andersson, 1994; Ho¨glund and Alatalo, 1995).
• This is paradoxical: variation should diminish rapidly due to
the directional selection imposed by female choice.
• Nevertheless, female choice persists and so does variation
in the male secondary sexual traits chosen by females.
• Maintenance of variation in the face of strong directional
selection is a general problem in evolutionary biology.
• Strong female choice with persistence of variation in male
secondary sexual characters on leks has led to the ‘‘lek
paradox’’ (Borgia, 1979; Taylor and Williams, 1982).
The Lek Paradox 3
• Here, we focus on the lek paradox in a
narrow sense, which is
most
– maintenance of variation in female choice
– and variation in male quality
– on leks and similar male aggregations
Black grouse
• Several different solutions are suggested
• Variation in male traits could be maintained through
– nonlinear selection for exaggerated traits (Pomiankowski and Møller, 1995, but
see Rowe and Houle, 1996)
– cyclic evolution of sexually selected traits due to intrinsically unstable Fisher’s
runaway processes (Iwasa and Pomiankowski, 1995)
– condition dependence of sexually selected traits (Rowe and Houle, 1996).
• Reproductive skew on leks may not be as high as thought because
females also mate with low quality males.
• Variation in male traits persists because there actually is no strong
directional selection on them.
Solutions to the Lek Paradox 1
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Randerson et al. (2000) said simple errors in mate choice maintain variation in mate quality.
Females may not be as choosy as typically thought if, for example, there is high predation
risk on the lek (Grafe, 1997).
Females may express age-specific preferences, increasing variation (Coleman et al., 2004).
Females may choose for compatible, rather than good, genes; each female has a different
optimal mate (Mays and Hill, 2004; Neff and Pitcher, 2005; Roberts and Gosling, 2003).
Selection for direct benefits, which may not necessarily correlate with indirect benefits,
could also lead to variation in female choice (Kirkpatrick and Ryan, 1991; Reynolds and
Gross, 1990; Williams, 1993).
Although lekking males are typically not thought to provide direct benefits to choosing
females, there may be reduced costs associated with choosing particular males.
Males may differ in their risk to females in terms of predation (on females or eggs),
reproductive parasitism, or harassment.
If high-quality bourgeois (territorial) males attract large numbers of predators, reproductive
parasites, harassing males, or pathogens (hereafter collectively referred to as enemies), then
females must trade-off the genetic benefits of mating with high-quality bourgeois males
against the costs imposed by enemies.
High-quality males may be riskier because they are more conspicuous (Breden and Stoner,
1987) or because they harbor higher densities of sexually transmitted pathogens or
ectoparasites (Kokko et al., 2002; Reynolds and Gross, 1990).
Solutions to the Lek Paradox 2
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high-quality males may be risky to females: mobile enemies may congregate around them,
even if they are no more conspicuous than lower quality males.
This argument assumes that mobile enemies can impose high costs on females.
– Clearly, predators on females or eggs will be costly.
– Brood parasites should also be costly to females if parasites kill or harm host offspring or if the
costs of parental care increase with brood size (e.g., in fish: Sato, 1986; Wisenden, 1999; in birds: Tewksbury et al.,
2002; in insects: Tallamy and Horton, 1990).
– Harassing males may impose energetic costs, disrupt matings, or injure females (e.g., Bro- Jørgensen,
2003; Magurran and Seghers, 1994; Schlupp et al., 2001; Shine et al., 2000; Stone, 1995; reviewed in Clutton- Brock and Parker,
1995).
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However, this has been rejected in several instances based on the observation that females
tended to congregate around males that bear high risks of harassment or parasitism or
because there was no correlation between harassment and mating (Carbone and Taborsky, 1995; Saether
et al., 1999).
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evidence that some females avoid sneakers, suggesting that the latter are costly to females
(Alonzo and Warner, 1999, 2000; van den Berghe et al., 1989; Warner and Hoffman, 1980; reviewed in Taborsky, 1994),
– Such costs may result from low genetic quality of sneakers (van den Berge et al., 1989), costs of
harassment (for references, see above), nest predation (van den Berghe et al., 1989), or negative brood
care responses of bourgeois males (Neff, 2003).
– The argument that females attempt to avoid parasitic or harassing males when making decisions
regarding mating on leks has been proposed previously (e.g., Alonzo and Warner, 2000; Clutton-Brock et al., 1992;
Taborsky, 1994).
Predators, reproductive parasites, and the
persistence of poor males on leks 1
• Hamilton, et al, 2005, presented several models suggesting that
avoidance of
Greater prairie chicken
• costly and mobile predators
• sneakers
• brood parasites (enemies)
leads to variation in female choice.
• This can result in maintenance of variation in male quality.
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Ian M. Hamilton, Marcel P. Haesler, and Michael Taborsky Department of Behavioural Ecology, Zoological Institute,
University of Bern,Wohlenstrasse 50a, CH-3032 Hinterkappelen, Switzerland
‘‘Enemies’’ congregate around higher quality males.
Female trades off benefits of high-quality males against risk
Predators, reproductive parasites, and the
persistence of poor males on leks 2
• At equilibrium, predict a positive correlation between quality of a
male and the proportions of both enemies and females visiting him.
– first model: bourgeois males ranked according to quality; use this framework to
predict the lowest quality male on the lek that will receive any matings, the
number of males that receive female visits, and the number of female visits
received by each male
– second model: consequences of female-enemy interactions on the success of
bourgeois males; influence on the maintenance of variation in male quality
• Low-quality males persist when enemies costly to females or occur at
high density, and when there is spatial structure on the lek, so
neighboring males typically of similar quality.
• If enemies are more costly to males than females, high-quality males
may benefit from receiving fewer female visits.
– third model considers special case: enemies are male reproductive parasites.
Predators, reproductive parasites, and the
persistence of poor males on leks 3
• These models illustrate the importance of considering the
simultaneous decisions of multiple players in mate choice games.
• Because the distribution of enemies will follow that of females, this
leads to some females preferring the ‘‘good’’ males as expected and
some visiting the low-quality males because they present a smaller
risk.
• This can promote the existence of ‘‘poor’’
males, despite a unimodal distribution of
female mating preference for indirect
(genetic)
benefits in the population.
Sage grouse (Jess Lee photos)
Polyandry
– Female associates with several males
– Parental care typically by males
– Fewer than 1% of all birds
Spotted sandpiper
Polyandry:
• evolved primarily in 2 orders of birds: Gruiformes &
Charadriiformes
• typically involves sex-role reversal (females larger & more
brightly colored)
• males incubate eggs & care for young
• examples include Spotted Sandpipers & the jacanas
• key factor in evolution of polyandry may be the fixed, four-egg
clutch of shorebirds:
– with a fixed clutch, the only way females can increase their
reproductive success (assuming favorable conditions) is to
lay more clutches
Photos © Natalie Demong
Jacanas,
Polyandry
and Fidelity
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Male Wattled Jacana would seem to be a loser in the genetic lottery. Seduced by a twotiming female and then abandoned to raise young that aren't his own
some of the young carry his genes, and other males raise young that he has sired.
Emlen et al. (1999) observed Panamanian jacanas, witnessing more than 1,400 copulations
between dominant females and much smaller males.
Males incubate eggs and raise chicks. Females are copulating with other males.
Jacanas females pair simultaneously with a harem of males who care for the young.
DNA revealed over 40% of broods included chicks fathered by a different male.
However, when no extra males were available in a harem, all chicks were sired by the caretaking male. Thus a male's risk of being cuckolded comes entirely from other males that are
simultaneously paired to the same female.
Jacanas,
benefits
Bronze-winged jacana
Jacana spinosa
• Emlen said biologists assumed males would only bear full parental responsibility
when there is certainty that the young are genetically his
• Instead, a male jacana sits on the nest, watching the female mate with other males
• Simultaneous polyandry is beneficial for female jacanas.
• "If a large, dominant female can maintain a harem," Emlen says, "her reproductive
success is enhanced by having lots of males raising young for her.
• Females benefit from pairing polyandrously; males, however, would avoid the cost
of cuckoldry if they paired monogamously.
• Why does the male jacana tolerate this behavior? In heavily populated and highly
competitive habitats with limited space for nests, some males never reproduce
• I guess you could say the males are lucky, considering the alternative," Wrege, a coauthor, says. "At least they're adding something of their own to the gene pool."
Comb-crested jacana
• http://pod.vodpod.com/video/1109-comb-crested-jacana-irediparra-gallinacea
Promiscuity
• Indiscriminant sexual relationships, usually of
brief duration
• About 6% of all birds
• Hummingbirds
– Male courts
– They mate
– Females builds nest, tends young
– A different male courts…
Extra-pair copulations (EPCs)
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have been reported in monogamous species, polygynous species, & polyandrous species
are also referred to as EPCs, and are defined as copulations with individual(s) other than a mate or
social partner. EPCs may result in extra-pair fertilizations (EPFs) which, in turn, may result in extrapair young (EPY). The percentage of EPY in populations may range from 0 to more than 50%. In
many songbird populations, the percentage of extra-pair young has been found to be about 10 25%, suggesting that at least some individuals in a population benefit from EPCs:
– Possible benefits of EPCs for males:
• Increased fitness
• Possible future mate acquisition
• Insurance against mate's infertility
– Possible benefits of EPCs for females:
• Fertility insurance
• Genetically diverse young
• Improved genetic quality of young
• Access to resources
Female barred owl being fed by male –
avoids EPCs by sequestering female
• http://www.youtube.com/watch?v=h1UXzK5ECbU
EPCs – possible costs
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Because, in most populations, many individuals do not engage in EPCs, such
behavior must also have costs:
Possible costs of EPCs for males:
– Sperm depletion & ejaculate production costs
– Increased risk of cuckoldry
– Reduction in parental care
– Increased likelihood of divorce
Possible costs of EPCs for females:
– Male retaliation
– Risk of injury
– Harassment from extra-pair (or potential extra-pair) males
EPC Prevention
• To maximize their own fitness (reproductive success), males try to
prevent their mates from engaging in EPCs. From an evolutionary
perspective, it simply doesn't pay to be cuckolded (that is, having a
mate engage in EPCs, and end up caring for another male's offspring).
To avoid being cuckolded, males may use paternity guards such as:
• Mate guarding
– males remain close to fertile mates to deter
other
males that might be seeking EPCs
– does not occur in all birds
– Costs of mate guarding include time,
energy, & opportunity costs
Mate guarding by male Bank Swallows
Males chase other females
several days before their
mates begin egg-laying
(when their mates are not
fertile). When their mates are
fertile (within a few days of
laying their first egg), males
chase their own females
almost exclusively. Then,
once egg-laying is nearly
finished (and mates are no
longer fertile), males again
chase other females. Open
circles = males chasing a
mate; closed circles = males
chasing females other than
their mate (From Beecher
and Beecher 1979
Frequent copulation among polygamous species
• With frequent copulation:
–probability of fertilization for a male
may be proportional to relative
number of sperm delivered to
particular female
–last male to copulate with a female
fertilizes more eggs
Why is there so much variation among & within species in
mating strategies?
• Costs & benefits vary among species
(e.g., importance of male parental care &
distribution of breeding territories)
• Costs & benefits vary among individuals
(e.g., with age and quality)
• Neodorf, Diane L. H. 2004. Extrapair paternity
in birds: understanding variation among
species. Auk 121: 302-307
Extrapair Fertilizations 1
• Hypotheses to Explain Variation in Extrapair Fertilizations among Species
• Breeding synchrony: Stutchbury and Morton (1995) proposed that
breeding synchrony promotes extra-pair fertilizations (EPFs) because
synchronous breeding allows females to more effectively compare
potential extrapair males that would be competing and displaying for
extrapair copulations (EPCs) at the same time.
• Others suggest asynchrony promotes EPFs: if males guard their
mates, asynchronous breeding allows opportunities to seek EPCs
when their own mates are not fertile.
• Although single species population-level studies have not supported
synchrony or asynchrony, comparative studies indicate a strong
relationship between synchrony and EPFs in certain species.
• Whether synchrony has resulted in the evolution of extrapair mating
systems or whether it correlates with a yet unknown factor remains
to be determined.
Extrapair Fertilizations 2
Breeding density: High breeding densities may
promote EPCs because opportunities for both males and females to
pursue EPCs should be much greater when individuals are nesting in
close proximity.
• However, this hypothesis has met with limited support from
intraspecific comparisons within and among populations.
• In a comparative analysis involving 72 species, Westneat and
Sherman (1997) found no relationship between nesting density and
EPF frequency.
• Nesting density may influence EPF frequency within populations of
some species, e.g., Eastern Bluebirds (Gowaty and Bridges 1991), but
does not appear to be a reliable predictor of whether a particular
species will have extrapair matings (Griffith et al. 2002).
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Extrapair Fertilizations 3
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Male parental care: There are two hypotheses regarding how levels of male involvement in
parental care may contribute to variation in EPFs among species
– First, males may be limited in their pursuit of extrapair matings because of constraints
imposed by caring for offspring – the trade-off hypothesis
– males may face a trade-off between caring for offspring and seeking extrapair mating
– Future studies examining male extrapair mating behavior during various nest stages
would be good tests of the trade-off hypothesis.
– Second, the female-constraint hypothesis; Gowaty 1996 proposes if males retaliate with
reduced parental care in response to low paternity certainty and females cannot
compensate for the loss, that females will be less likely to seek EPCs.
– The few experimental tests of the female-constraint hypothesis have mixed results.
– Findings from comparative studies provide support for female-constraint hypothesis.
– Using removal studies, Arnold and Owens (2002) found a significant negative correlation
between necessity for male care and EPF frequencies among species and concluded
that, in species where females are able to compensate for loss of male provisioning,
EPFs are more common.
– If male care is essential, extrapair paternity should be less likely.
Extrapair Fertilizations 3
• Genetic variability within populations: If females are seeking indirect
benefits from extrapair matings (i.e. good genes or genetic
heterozygosity), genetic variability among males in a population is
predicted to affect female benefit.
• If there is little genetic variation among males, females would not
benefit from seeking EPFs (Petrie and Kempenaers 1998 ).
• In a comparative study, Petrie et al. (1998) found a significant positive
relationship between EPF frequency and estimates of genetic
variability.
• Further tests of this hypothesis are needed that involve comparisons
among populations of species where males differ in levels of genetic
variability.
EPC: Where Do We Go From Here?
• We currently have no single reliable predictor of
whether or not a species will adopt an extrapair
mating strategy.
• Some strong correlations have been identified,
but many exceptions exist.
• Understanding the evolution of avian extrapair
mating systems remains an exciting and
enigmatic area of research.
Mean ± SE onset of dawn song in Blue Tits for (a) males that did or did not gain
extrapair paternity (EPP) and (b) males that lost paternity (cuckolded) or did not lose
paternity in their own nest. Sample sizes are shown above data points.
Early birds are sexy: Blue Tits 1
http://www.youtube.com/watch?v=WCGi8uhFTu4
• Sexual selection theory predicts signals reflecting relative quality of
individuals should be used in mate choice.
• Females could base their choice of copulation partners on male
secondary sexual traits that honestly signal male age, as predicted by
the age-based indicator mechanism.
• Studies have shown that female blue tits prefer older males and that
aspects of dawn song reflect male quality, but it remains unknown
whether dawn song characteristics correlate with male age.
• Poesel et al. (2006) compared dawn song characteristics of secondyear (SY) and older (ASY) male Blue Tits, and tested for age-related
changes and differential overwinter survival of SY males.
Early birds are sexy: Blue Tits 2
• They also investigated the relation between dawn song and paternity
gain and loss
• ASY male Blue Tits began to sing earlier relative to sunrise than did SY
males.
• This difference in the onset of dawn singing was due to age-related
changes in individual performance rather than differential survival of
individuals with varying expression of the trait.
• Males that began to sing earlier had more mating partners, and were
more likely to gain extrapair paternity.
• These findings suggest that the onset of dawn song can provide a
simple mechanism for females to assess the relative quality of their
mate and of neighbouring males.
• Female Blue Tits appear to use the onset of singing as a cue for their
choice of extrapair partners.