Transcript Inter-sexual selection

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 malemale 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 are relatively
unselective in mating,
whereas females are
more choosy
Males have greater
reproductive
potential, provide
less parental care
Males compete more for
females than vice versa
Evolution of traits in males (size, color, song) that enhance
competitive ability or signal condition, resources
Reproductive effort = parental effort + mating effort
Parental effort
Mating effort
Males
Females
Mating
system
Monogamous
Polygynous
Intensity of
sexual selection
Weak
Strong
Constraints
(ecological, social, physiological)
Males freed from parental care
Intense competition for mates
Strong sexual selection
Pronounced sexual
dimorphism
Males’ parental care essential
Less intense mate competition
Weaker sexual selection
Less pronounced
sexual dimorphism
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
Reproductive skew in satin bowerbirds
Females: # of mates
Males: # of mates
Reproductive skew in male baboons
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
Baboon sexual consortships
• 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
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’.
20 m
Female copulation call
20 m
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
# looks toward speaker
5
4
Male speaker
Female speaker
3
2
1
0
% approach speaker
80
60
40
20
0
During
consort
Test
Other
male
Control 1
After
consort
N = 9 subjects
Control 2
Crockford et al. 2007, Anim. Behav.
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)
Constraints
(ecological, social, physiological)
Males freed from parental care
Intense competition for mates
Strong sexual selection
Males’ parental care essential
Less intense mate competition
Weaker sexual selection
Pronounced sexual
Dimorphism
Less pronounced
sexual dimorphism
POLYGYNY
MONOGAMY
Degrees of polygyny in mammals
Slight polygyny:
lions
More polygyny:
gorillas
Extreme polygyny:
elephant seals
M:F body wt
1.3/1
2.3/1
3.1/1
• 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
Most studies
address only some
of these questions!
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
 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
Growth and song development in swamp sparrows
Control group = 9
Experimental group = 7
fed 70% of food
Cross-correlation score
Song-copying fidelity
0.7
0.6
0.5
0.4
0.3
Control
Nowicki et al. 2002. J. Comp. Physiol. A
Experimental
Mean # nests per male
2
Mean # nests per male
Mate choice and tail length in widowbirds
2
Before
1
0
After
1
N = 9 birds in each treatment
0
Shortened Control 1 Control 2 Elongated
Tail treatment
Andersson 1982, Nature
Responses of female house finches to males of
different plumage color
Mean rank of male
4
3
O
O
2
Y
1
R
0
Yellow
Orange
Orange-Red
Red
O-R
Hill 1990
Simulated contests between male chickadees
Frequency (kHz)
Submissive playback
Aggressive playback
5
5
4
4
3
3
2
2
1
1
0
0
1
2
Time (sec)
3
4
0
0
1
2
3
Time (sec)
4
Simulated contests between male chickadees
Wimp!?!
Neighbor
Mate
Female
Aggressive
playback
Female
then:
Intruder
Intruder
My hero!
Mate
Neighbor
Female
Subordinate
playback
Intruder
Female
then:
Intruder
Female chickadees prefer to mate with high-ranking males
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.
0.6
% of nests containing
extra-pair young
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.
High-ranking males
23
0.4
0.2
10
10
0
Test:
Aggressive
Playback
Control:
Submissive
playback
Control:
No playback
Mennill et al. 2002, Science
 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
Mate sampling by some birds
Peacocks
Reed warblers
Pied flycatchers
Mean #
visits
3
6
3
Choice based on:
eye spots (tail length)
song length
multiple: mating status: 91%
plumage: 64%
nest quality: 73%
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?
Stickleback fish
However, females often seem to prefer even more extreme
versions of the trait (e.g. widowbirds)
Bakker 1993
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.)
Female choice in poison dart frogs
Epipedobates tricolor
Dendrobates leucomelas
• 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)
Forsman & Hagman 2006, Evolution
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?
Mating success
Barrier removal experiment
Time
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
No. of individuals
Female
preference
Costs (e.g. predation pressure)
Bright
Dull
Male coloration
Optimum, natural
selection
Optimum,
female choice
XX
XX
“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?
Guppies
Predation
12
High
Medium
Low
Spots per fish
11
10
9
8
7
Streams
Endler 1980
Guppies
Spots per fish
Rivulus (predator on
juveniles)
Control
12
Crenicichla (predator on
adults)
Start of
experiment
10
8
0
2
4
6
8
10
12
14
16
18
20
Months
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