Mating Systems IV:Leks (Part B), Polyandry

JodyLee Estrada Duek, Ph.D.With assistance from Dr. Gary Ritchison

http://people.eku.edu/ritchisong/matingsystems.html

Spotted sandpiper

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

most narrow sense, which is – maintenance of variation in female choice – and variation in male quality – on leks and similar male aggregations

• 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.

Black grouse

Solutions to the Lek Paradox 1• 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• 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).

• 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).

• 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 thepersistence of poor males on leks 1

• Hamilton, et al, 2005, presented several models suggesting that avoidance of • costly and mobile predators• sneakers• brood parasites (enemies) leads to variation in female choice.

• This can result in maintenance of variation in male quality. • 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

Greater prairie chicken

Predators, reproductive parasites, and thepersistence 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 thepersistence 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

Jacanas, Polyandry

and Fidelity

• Male Wattled Jacana would seem to be a loser in the genetic lottery. Seduced by a two-timing 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 care-

taking male. Thus a male's risk of being cuckolded comes entirely from other males that are simultaneously paired to the same female.

Photos © Natalie Demong

Jacanas, benefits

• 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

co-author, says. "At least they're adding something of their own to the gene pool."

Bronze-winged jacanaJacana spinosa

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) • 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 extra-pair 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• 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 SwallowsMales 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).

Extrapair Fertilizations 3• 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

• 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 second-year (SY) and older (ASY) male Blue Tits, and tested for age-related changes and differential overwinter survival of SY males.

http://www.youtube.com/watch?v=WCGi8uhFTu4

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.