Mating Systems in Birds III: Polygyny , Leks (Part A)

Mating Systems in Birds III: Polygyny, Leks (Part A) Acrocephalus palustris, Marsh warbler • JodyLee Estrada Duek, Ph.D. • With material from Dr. Gary Ritchison Dr. Robert Payne • http://people.eku.edu/ritchisong/matingsystems.html • http://elibrary.unm.edu/sora/om/om033.pdf

Evolution of breeding systems in Acrocephalinewarblers • Comparative analyses important to studies of adaptive behavior. • Previous studies of avian mating systems considered paternal care and habitat type and evolution of polygyny. • Leisler et al. (2002) extended those studies and included analyses of habitat quality, characterized by food supply. • Species in the monophyletic lineage of acrocephaline warblers (Acrocephalus, Chloropeta, Hippolais) are widely distributed, inhabit a variety of different habitats, and show a variety of breeding systems. • Using molecular phylogeny, Leisler et al. (2002) reconstructed patterns of changes in 17 species from social monogamy to polygyny, and in paternal brood care. • Analyzed the coevolution of brood care participation of males and social system, how it relates to habitat quality, and assessed the phylogenetic inertia of mating systems. • Support the hypothesis that change to highly productive habitats associated with a greater emancipation of males from brood care, and with polygyny and promiscuity. • Poor habitats were associated with monogamy and nest helpers. • In contrast to morphological characters, mating systems phylogenetically labile.

Paternal care and food resources Phylogenetic analysis of the relationship between paternal care and food supply of six species of acrocephaline warblers. Paternal care data were square-root-arcsine-transformed prior to analysis. The regression through the origin was associated with a correlation of r = -0.859, P < 0.0001. (Leisler et al)

Polygyny • Male mates with several females (but each female mates with only one male) • Parental care usually by female • only about 2% of all birds • Common in groups where a male holds a territory • Elephant seal • Lion • Some reef fish • Three major types of polygyny

Polygyny • Resource defense polygyny: monopolize territory or resource (indirect polygyny) • Female defense polygyny: (harem or direct polygyny) monopolize females • Male-dominance polygyny: males sort themselves through dominance or display (includes leks)

Polygyny • Some males in a population regularly have two or more mates • In North America, 14 of 278 breeding songbird species (11 of which nest in marshes or grasslands) are polygynous • Examples include Red-winged Blackbirds & Marsh Wrens • Why should a female pair with an already mated male while there are still unmated males available? • This question is addressed by the 'polygyny threshold model'

Predictions of the Polygyny Threshold model • A male's territory quality will be correlated with his mating success • demonstrated in Dickcissel, Bobolink, & Lark Bunting • Polygyny should be more common in patchy environments (where there is more variation in territory quality) • Verner & Wilson (1966): compared habitats & mating systems in North American passerines • 14 polygynous species & 13 of 14 occur in marsh or grassland habitats ('patchy' habitats with much variation in productivity/quality)

Male dominance polygyny • Males compete for 'status' in communal displays (leks) & females choose among males • Females get only sperm from males (they raise young elsewhere unaided by males) • Much variation in male mating success (one or a few males copulate with many females; other males with none)

Leks and lekking • A lek consists of clustered male territories that females visit (lekking ground) strictly for the purpose of mating (there is no male parental care in lekking species). • Male territories therefore do not hold resources attractive to females other than the males themselves. • Leks are characterized by • (i) male clustering • (ii) extreme bias in female choice, resulting in skewed male mating success • (iii) stability of lek location over time.

Theoretical models for leks 1 • Four theoretical models have been proposed to account for the origin and maintenance of leks: • female preference • hotspot • hotshot • black hole models • Each has been validated in particular cases, and most are not mutually exclusive; therefore, it has been difficult to contrast and separate them, empirically and experimentally.

Theoretical models for leks 2 • female preference - preference forclumped males,with an increased percapita male mating successin larger leks. • Females may preferclustered males for differentreasons, for example, • reducedcosts of mate sampling • higher absolute quality ofthe best male inlarger groups • deflectionof predators from nestsites. • 'hot spots' - males gather where females are likely to congregate • 'hot shots' - females prefer to choose mates from aggregations of males (i.e., group displays facilitate comparisons) • black hole - females arehighly mobile, moving withinhabitat and matingwith male inwhose territory they finallyhappen to be present.There is no femalepreference for a particularkind of male orlek size.

Manipulating lek size and composition using decoys • By using decoys to mimic natural leks in the Little Bustard, artificial leks attracted wild birds. • Then, by manipulating artificial lek size and structure (sex ratio, male phenotype), responses of wild males and females allowed Jiguet and Bretagnolle (2006) to test specific predictions derived from the four classical models of lek evolution. • The hotspot model not supported: female decoys did not attract wild males. • Conversely, hotshot males do exist in this species (attracting females and males) • a female preference exists for a particular lek size (four males). • Finally, males aggressive toward decoys attracted fewer females, consistent with one of the mechanisms by which the black hole model may work. • Therefore, three models of lek evolution were partly or fully supported by our experimental results: hotshot, female preference, and black hole models. • We suggest that these models actually fit within each other, ensuring the evolution, functioning, and long-term maintenance of leks.

Wild male Little Bustard (left) visiting a male decoy (right) on an artificial lek; female Little Bustard visiting a male decoy (Photos by F. Jiguet).

Carotenoids and antioxidants 1 • Carotenoid-based signals thought to be indicators of quality because must be dietary; mightindicate ability to gather high-qualityfood. • Carotenoids also known to have importantphysiological functions as immunoenhancers and antioxidants; carotenoid-based sexual traits have been suggestedto reflect health and antioxidant status • Hypothesis: carotenoids allocated to sexual signals are no longer available forthe detoxification system. • Recently challenged: antioxidant activity is notmain biological role of carotenoids. • Instead, carotenoid-basedsexual traits might signal availability of other non-pigmentaryantioxidant molecules that protect carotenoids from free radicals and make them available for sexual advertisements • Because carotenoids are very sensitive to oxidation that alters and destroys their color, theirsignalling function can only be ensured if they are protectedfrom the oxidation.

Carotenoids and antioxidants 2 • Hartley and Kennedy (2004) suggested that onlyindividuals that have a very effective antioxidant machinery(vitamins C and E, catalase, superoxide dismutase) would haveenough unbleached carotenoids available for the sexual signal. • Therefore, although carotenoid-based signalsmight still indicate the overall antioxidant status of theirbearer, the mechanisms would be slightly different from theone originally envisaged.

Carotenoids and antioxidants 3 • Bertrand et al. (2006) tested this hypothesis with Zebra Finches, a passerine specieswith a carotenoid-based signal: the color of the bill. • They simultaneouslymanipulated the availability of carotenoids and of a non-pigmentaryantioxidant (melatonin) in the drinking water. If the antioxidantproperties of melatonin protect carotenoids from oxidation,birds supplemented with melatonin should haveredder bills than birds not supplemented with melatonin, andbirds supplemented with carotenoids and melatonin shouldhave redder bills than birds supplemented with carotenoids alone. • The findings of Bertrand et al. (2006) are in agreement with these predictions because carotenoidand melatonin supplementation had an additive effect on billcolor. • The first experimental evidencethat a non-pigmentary antioxidant enhances expression ofa carotenoid-based sexual trait.

Changes in bill color scores of male Zebra Finches of different supplementation groups. Values are means ± 1 SE (N = 40). Changes were computed as the differences between the final and the initial values of bill color scores for each group (From: Bertrand et al. 2006)

Source: http://www.cs.uwindsor.ca/users/m/mweis/public/55-324/lectur11.htm

Male dominance polygyny • Examples include Sage Grouse, Prairie Chickens, several species of Manakins (see 'The Dance of the Manakin'), & several Birds-of-Paradise • Characteristics that appear to influence a male's mating success: • Age, experience, & status • by mating with dominant male, females may obtain for offspring the genes responsible for a male's superior traits • females may judge male quality based on quality of plumage or displays (better plumage & displays = healthier male, i.e., a better forager or less susceptible to parasites/infections) • Sharp-tailed grouse http://www.youtube.com/watch?v=EZmI7f4TcPs

Development of coordinated singing in cooperatively displaying Long-tailed Manakins • Long-tailed manakins (Chiroxiphia linearis) have a puzzling social system in which teams of two males display cooperatively in dispersed lek arenas, but only the alpha partner mates • One benefit of performing as a nonmating partner might be to gain experience as an "apprentice" to improve performance of the complex duet song and joint dance. Trainer, J.M., D.B. McDonald, and W.A. Learn. 2002. Behavioral Ecology 13: 65-69.

Long-tailed Manakin 2 • Video of dual-male dance display of Long-tailed Manakins in Monteverde, Costa Rica. In this clip, two definitive-plumaged males (likely 10 years old or older) dance for two green females. Only the alpha male will mate with one of these two females. The other female will likely return to copulate with the alpha later the same day or in succeeding days. These particular males were incredibly successful that year (1998). For every 2-hour observation session we conducted that season, the alpha copulated at least once. • http://www.uwyo.edu/dbmcd/lab/LTMvideo.htm

Long-tailed Manakin 3 • Trainer et al. (2002) examined the relationship between the age of singers and two measures of singing performance: • song variability • sound frequency matching. • Singing performance improved with age; variability in four song characteristics of males less than 3 years old was greater than that in their older partners, and frequency matching increased with the age of the younger partner. • Randomization tests of song samples from seven well-established teams showed that males did not track the song-to-song variation in their partners’ singing. • Another randomization test showed that frequency matching by these teams was higher than that of randomly paired partners. • It is a “set performance” rather than a team that might improvise

Long-tailed Manakin 4 • They considered three alternative hypotheses for congruent songs: • short-term accommodation to the partner’s song • active choice of partners with similar intrinsic frequencies • long-term development of congruent song through practice or song copying • Long-term monitoring of banded birds supports the hypothesis that frequency matching develops over several years during the complex and protracted process of partner formation • Nonmating males may benefit from increasing their competence at display, eventually enjoying increased mating success when they inherit display sites from older males (apprenticeship) • [Behav Ecol 13:65-69 (2002)]

Judging male quality • Pheasant sexual selection & displays • (Attenborough) http://www.youtube.com/watch?v=mNXgh333ihQ

Alternative Strategies in a Lek 1 • In arena species, are males that are not aggressive or that do not display nevertheless successful in mating? • Alternative mating strategies within a species are well known in certain insects (Blum and Blum 1979; Thornhill 1979)and fish (Loiselle and Barlow 1978; Dominey 1980; Gross 1982), but are uncommonly mentioned in birds(Krebs and Davies 1981). • Independent males: do not attend the lek • Satellite males: hang around lek edges, seldom display • Sneaker males: something completely different • May be labile strategies, depending on age, season, competition

How does a male decide? • Males of many vertebrate species have flexible reproductivephenotypes and must decide before each mating season whetherto adopt sneaker, satellite, or territorial mating tactics. • Testosterone levels have measured highest in territorial males, then satellite males, with sneaker males having the lowest levels. • Among iguanas either blocking or injecting testosterone resulted in behavioral changes. • Martin Wikelskia, Silke S. Steigerb, Bernhard Gallc and Karin N. Nelsond , Behavioral Ecology 2005 16(1):260-268

Alternative Strategies in a Lek 2 • From Payne, 1984: Lekking Ruffs are the only birds known to have apparently genetically-determined differences in sexual behavior. • Certain males are not aggressive like the displaying males in the lek, and they court females away from a lekking ground, visit several lek arenas, and remain around the edge of a lek as "satellites" (Hogan- Warburg 1966; van Rhijn 1973). • These satellite males and the aggressive males have similar plumages, except that most satellites have a whitish neck ruff and head tufts. They sometimes mate with females at lekking grounds. • The fact that they are different in plumage suggests that their behavior also may represent a genetic morph. Adult males can develop female-like plumage in captivity (Stonor 1937), but are not known to do so under field conditions.

Alternative Strategies in a Lek 3 • (Payne 1984) occurrence of non-displaying males near active leks suggests alternative mating styles in other species. • Male grouse (Black Grouse; Sharp-tailed Grouse) sometimes attract a female and copulate away from a lek (Hjorth 1970; Kruijt et al. 1972; Sexton 1979). • In Paradisaea birds of paradise, males in "immature" or "female-like" plumage display like the plumed males and on occasion mate with females visiting a lek (Wallace 1869; LeCroy et al. 1980). • Female-like male riflebirds (Ptiloris victoriae) sometimes display to a female near an adult male on an arena (Schodde 1979). • Female-like plumages are known in some other birds of paradise (Gilliard 1969) and in a few other lekking birds: manakins (Snow 1963; Sick 1967) and arena bellbirds (D. W. Snow 1973a). • Female- or immature-plumaged male manakins sometimes display in leks, sometimes away, and may or may not have large testes (Sick 1967; D. W. Snow 1977). • Young male Satin Bowerbirds are in female-like plumage for the first few years of life. They visit the arenas, where they are attacked by the older resident male, probably because they are a sexual threat (Vellenga 1970, 1980b).

Alternative Strategies in a Lek 4 • (Payne 1984) The plumages of these subadult males lack the bright colors of the lekking males, and so lack the signals that elicit attack by the resident males (e.g., Rohwer et al. 1980). • The aggressive behavior of adult Satin Bowerbirds toward younger visitors at the arena, however, casts doubt on the predictiveness of this female mimicry hypothesis insofar as young males lack the plumage colors of the resident adults, yet are vigorously attacked. • The scarcity to date of observations of mating by males in subadult plumage suggests that the alternative strategies are not important, in general, and that the elaborate bright colors and large sizes of male lek birds are often an evolutionary result of social competition.

Female mimics in a lekking shorebird • Female mimics are known from many species, but permanent, non-conditional, alternative mating strategies are known from an isopod, a fish, a lizard and a bird. • The bird example: lek-breeding Ruffs (Philomachus pugnax), a shorebird for which two strategies (independent and satellite) have been known for over 50 years. • Ruffs also provided the single case of an animal with two, rather than three, permanent alternative mating strategies. • Jukema and Piersma (2006) described a rare female-like morph of Ruffs: the ‘missing’ third alternative mating strategy that they called ‘faeder.’ • Faeders are slightly larger than females and have testes 2.5 times the size of testes of normal males. • On leks in aviaries and in the wild, they appear to combine feminine and masculine behaviors. • Faeders may represent the ancestral, care-giving, male strategy, but their relatively large testes suggest that currently they behave as sneakers.

A female mimic (or faeder) • on the left are two female mimics, on the right a typical male, and between them a single female • a female mimic being mounted by a male • [Photos by J. and T. Champion (a & c) and Y. Verkuil (b)].

Figure 2. (a) Relative frequency distribution of wing lengths of the three categories of ruffs captured during northward migration in the northern Netherlands (2001–2004). Of the 20 birds with wing lengths between 170 and 180 mm, 11 were bled and in all cases they were molecularly confirmed to be males; the sex of 25 additional females and 28 males was also molecularly confirmed.

Figure 2: (b) Samples of breast feathers of the nuptial plumage of two typical males (top), two female mimics or ‘faeders’ (middle row) and two females (bottom) of ruffs staging in April in The Netherlands. In female mimics and females these feathers represent the original alternate plumage, in males an additional, supplementary plumage (Jukema & Piersma, 2000)

Mating Systems in Birds III: Polygyny , Leks (Part A)