Most mammals are polygynous Males contribute comparatively little parental care Males are typically larger than females Males typically have more ‘weapons’ than females Most birds are monogamous Males and females contribute relatively equally to parental care Males and females are the same size and color But in polygynous bird species, males (like male mammals) contribute relatively little parental care They are also usually more brightly colored and ornamented than females Why?

Why, in most mammalian species, are males larger than females and why do males have more ‘weapons’? Why are males more brightly colored and ornamented than females in some species but not others? Why is sexual dimorphism usually greater in polygynous species than in monogamous species?

: Sexual selection: Selection favoring traits that give certain individuals an advantage over others in obtaining mates Intra-sexual selection favors traits that affect the ability of members of the same sex to compete with each other for mates (usually concerns male- male competition) Inter-sexual selection favors traits that attract members of the opposite sex (usually concerns female choice of males)

Physiological differences between males and females in reproduction Males have greater reproductive potential, provide less parental care Males compete more for females than vice versa Males are relatively unselective in mating, whereas females are more choosy Evolution of traits in males (size, color, song) that enhance competitive ability or signal condition, resources

Parental effort Mating effort Males Females Mating system Intensity of sexual selection MonogamousPolygynous Weak Strong Reproductive effort = parental effort + mating effort

Males freed from parental careMales’ parental care essential Intense competition for mates Less intense mate competition Strong sexual selection Weaker sexual selection Pronounced sexual dimorphism Less pronounced sexual dimorphism Constraints (ecological, social, physiological)

Male-male competition in elephant seals  8 males fertilized 348 females (1:43.5)  Breeding season 3 months long, favoring male endurance  Males lose 34-41% of body mass

Females: # of mates Males: # of mates Reproductive skew in satin bowerbirds

Reproductive skew in male baboons

In species in which mating is monopolized by the biggest, strongest males, subordinate males must try to adopt alternative mating strategies One widespread strategy: ‘sneaky’ mating

a temporary pair bond between a male and a sexually receptive female characterized by close spatial proximity and mate-guarding usually, but not always, involves the alpha male Baboon sexual consortships

Sexual consortships are unstable and transient: marked by close spatial proximity last from several hours to several days Males who cannot compete with more dominant individuals try to take advantage of temporary separations between the consort pair to mate ‘sneakily’.

Female copulation call Male grunt During consortship: Test: Female’s call + consort male’s grunt Control 1: Female’s call + another dominant male’s grunt As soon as possible after consortship ends (the female is now consorting with a different male): Control 2: Female’s call + consort male’s grunt Prediction: Males will respond strongly in the test condition, weakly in the two control conditions 20 m

# looks toward speaker Male speaker Female speaker During consort Other male After consort Test Control 1 Control 2 Crockford et al. 2007, Anim. Behav. N = 9 subjects % approach speaker

Intra-sexual selection: two points 1.Big males don’t necessarily have big sons. Body size depends on age and condition in addition to genes. 2. Big dominant male can coerce females to mate. Yet it might also be in the interest of females to do so, because of: genetic quality protection, resources paternity confusion (to avoid infanticide)

Males freed from parental careMales’ parental care essential Intense competition for mates Less intense mate competition Strong sexual selection Weaker sexual selection Pronounced sexual DimorphismPOLYGYNY Less pronounced sexual dimorphismMONOGAMY Constraints (ecological, social, physiological)

Degrees of polygyny in mammals Slight polygyny: lions More polygyny: gorillas Extreme polygyny: elephant seals 1.3/1 2.3/1 3.1/1 M:F body wt

Female reproductive success is largely determined by parental effort Male reproductive success is largely determined by mating effort Because females invest much time and energy in offspring, a wasted mating is costly Therefore, females are predicted to be more choosy than males in selecting mates

Female choice of mates: * What criteria do females use in choosing mates? (e.g. resources, parental care, ‘good genes’) * How important has female choice been in the evolution of male traits that are: *not used in male-male competition? *costly in terms of the male’s survival? (e.g. the peacock’s tail)

Questions to be addressed: 1. Does the trait vary among males? 2. Is the trait an honest reflection of male quality? Is it costly? 3. Do females prefer males with extreme versions of the trait? 4. Do females sample among males? 5. Is there a genetic correlation between the male trait and female preference? 6. Do females benefit from mating with males with extreme versions of the trait? a. Males with the trait provide direct benefits (paternal care): protection, territory, feeding b. Males with the trait provide indirect (genetic) benefits** I. Sons are attractive (‘sexy’): mating advantage II. Offspring survive at higher rates: good genes ** males might also provide direct resources, but indirect benefits are easier to measure if there is no paternal care Most studies address only some of these questions!

1. Does the trait vary among males? 2. Is the trait an honest reflection of male quality? Is it costly? Reliable cues that cannot be faked: The trait may seem arbitrary (bright colors, elaborate song) but the condition it indicates is not The trait is condition-dependent Males in poor condition do not develop the trait fully Males often lose the trait after the breeding season

Control group = 9 Experimental group = 7 fed 70% of food Growth and song development in swamp sparrows Nowicki et al J. Comp. Physiol. A Control Experimental Song-copying fidelity Cross-correlation score

Before After Tail treatment Mean # nests per male Andersson 1982, Nature N = 9 birds in each treatment Mate choice and tail length in widowbirds

Responses of female house finches to males of different plumage color Mean rank of male Hill 1990 O R O-R Y O

Frequency (kHz) Time (sec) Submissive playback Aggressive playback Time (sec) Simulated contests between male chickadees

Female Intruder Mate Simulated contests between male chickadees Female Intruder Neighbor Aggressive playback Female Intruder Mate Female Intruder Neighbor Subordinate playback then: Wimp!?! My hero!

Test: Aggressive Playback Control: Submissive playback Control: No playback % of nests containing extra-pair young High-ranking males Mennill et al. 2002, Science Females with high-ranking mates are likely to mate ‘sneakily’ with a neighboring male if they perceive that their mate is now subordinate to the neighbor. There is no change in the behavior of females whose mates are already low-ranking, presumably because they already know that their mates are low-ranking. ~50% of all chicks are fathered by neighbors in all 3 conditions. Female chickadees prefer to mate with high-ranking males

4. Do females sample among males? How might females sample? Threshold: choose the first male that meets criteria Sequential: sample males as long as they are increasing in quality, then drop back to next to last male Sample among a pool: requires memory and ability to compare, revisit Copy other females In practice, sampling is costly. This may constrain choosiness

Mean # Choice based on: visits Peacocks 3eye spots (tail length) Reed warblers 6song length Pied flycatchers 3multiple: mating status: 91% plumage: 64% nest quality: 73% Mate sampling by some birds

Constraints on females’ sampling abilities constrain the strength of sexual selection If there is little cost to sampling, females can afford to seek the the ‘best’ male However, there are often are costs, particularly when males provide direct benefits (territory, paternal care) Females may choose ‘lesser’ males if: the male is already mated; other females already occupy his territory and paternal care it is dangerous/energetic costly to sample widely, especially when the breeding season is short In practice, females tend not to sample as much as is optimum for ‘perfect’ mate choice Sampling is more feasible when males provide no direct benefits

~ 5. Is there a genetic correlation between the male trait and female preference? Bakker 1993 Stickleback fish However, females often seem to prefer even more extreme versions of the trait (e.g. widowbirds)

Do females ever choose males on the basis of genes only (indirect benefits)? To answer this question, it’s most practical to focus on species where males provide no direct benefits (paternal care, territory, etc.)

Males call to attract females Male calling improves with age, suggesting that better calling signals higher survivorship In the wild, males care for young (by tending eggs in leaf litter and carrying tadpoles to puddles) However, in these experiments, tadpoles were raised without parents in identical conditions to control for parental effects (so any differences should be genetic) Dendrobates leucomelasEpipedobates tricolor Forsman & Hagman 2006, Evolution Female choice in poison dart frogs

FEMALE PREFERENCE FOR TRAIT TRAIT INDICATES QUALITY Forsman & Hagman 2006, Evolution

Peacocks with many eyespots are healthier

Do male ornaments signal good genes?

Satin bowerbirds: No male PI, high male reproductive skew, sexual dimorphism Elaborate nests Large brains Long lifespan* (7-21 years) Long development* (don’t start breeding until ~ 7 years) Blue objects are rare* Males steal from other males* Is mating success related to problem solving abilities?

Time Mating success Barrier removal experiment Red covering experiment Males significantly more likely to cover red. Related to mating success? Keagy et al. 2009, Anim. Behav.

How does sexual selection operate? How does it interact with natural selection? If the male trait and the female’s preference are heritable, the ‘trait’ gene and the ‘preference’ gene may become linked Female choice may drive the male trait beyond the optimum point in terms of natural selection High quality males should be able to overcome at least some of this cost

Female preference Dull Bright Male coloration No. of individuals Optimum, natural selection Optimum, female choice Costs (e.g. predation pressure)

“Indicator” theories of sexual selection XX

Runaway (Fisherian) sexual selection: 1. Females initially prefer males with a given trait because it signals high quality 2. Females who mate with these males produce sons with the trait and daughters with a preference for the trait 3. Female choice may drive the male trait beyond the optimum point in terms of natural selection 4. A runaway process occurs, where males with the trait are preferred only because they have the trait. 5. ‘Sexy’ sons have high reproductive success, even though they may not be in good condition. 6. Daughters obtain no benefits other than a preference for the trait.

Problems with runaway sexual selection theory: ‘Sexy” sons are primarily advantageous if: the sexy trait is relatively rare the trait isn’t too negatively correlated with offspring survival (especially of daughters) female choice isn’t too costly There is more opportunity for a runaway process if males provide no direct benefits If males with extreme versions of the trait are less fit, a female may do better to mate with a slightly less ‘sexy’ male whose offspring are more likely to survive.

Indicator (‘Good genes’/Handicap) models of sexual selection 1. Females initially prefer males with a given trait because it signals high quality (like runaway) 2. Females who mate with these males produce sons with the trait and daughters with a preference for the trait (like runaway) 3. Female choice may drive the male trait beyond the optimum point in terms of natural selection (like runaway) 4. High quality males should be able to overcome at least some of this cost 5. Costly male traits are preferred by females because they indicate fitness (even if it’s not always highly heritable) 6. Females who mate with such males produce both fitter sons and fitter daughters

Run.Ind. 1. Does the trait vary among males? 2. Is the trait an honest reflection of male quality? Is it costly? 3. Do females prefer males with extreme versions of the trait? 4. Do females sample among males? 5. Is there a genetic correlation between the male trait and female preference? 6. Do females benefit from mating with males with extreme versions of the trait? a. Males with the trait provide direct benefits (paternal care): protection, territory, feeding b. Males with the trait provide indirect (genetic) benefits** I. Sons are attractive (‘sexy’): mating advantage II. Offspring survive at higher rates: good genes

Run.Ind. Is the trait an honest reflection of male quality? Is it costly? Males with the trait provide direct benefits (paternal care): protection, territory, feeding Males with the trait provide indirect (genetic) benefits** I. Sons are attractive (‘sexy’): mating advantage II. Offspring survive at higher rates: good genes

A male trait can function both to attract females and to compete with rival males Male song in birds: broadcast to male for territory defense, directed at females for mate attraction Mane color in lions: signal of status to males, attractive to females

What is the relation between sexual selection and natural selection?

Predation High Medium Low Guppies Streams Spots per fish Endler 1980

Control Start of experiment Crenicichla (predator on adults) Rivulus (predator on juveniles) Guppies Spots per fish Endler 1980

Guppies in Trinidad Male ornamentation is important for female choice, but not for male-male competition. There may be a genetic correlation between female choice and male ornamentation. Ornamentation may reflect male quality: *Diet *Parasite load *Predation risk

Inter-sexual selection: Summary Inter-sexual selection generally concerns female choice Females may base their choice on: * direct examination of resources * male traits that are correlated with resources * male genetic quality independent of resources Male ornaments are not arbitrary, but have probably evolved because females use them as reliable indicators of male resources and/or genetic quality Inter-sexual selection (female choice) does not always reaffirm the results of intra-sexual selection (male-male competition) or natural selection It can lead to the evolution of male traits that are costly in terms of fighting and/or survival