Chapter 11 The evolution of mating
systems
Monogamy: one male one female
Polygamy
Polygyny: one male, multiple females.
Polyandry: one female, multiple males.
Polygynandry: multiple males, multiple
females.
Monogamy
Prolonged, essentially exclusive bond
maintained with one member of opposite sex.
Generally a rare system.
Rare in mammals (except for some rodents,
primates and dogs).
However, is commonest avian mating system.
Monogamy armed compromise rather than
happy collaboration.
Males would generally like to seek extra mates.
Why don’t they?
Several hypotheses:
Mate-guarding hypothesis
Mate assistance hypothesis
Female enforced monogamy
Mate guarding hypothesis (MGH)
Monogamy may be best choice if female
would mate again if male deserted her and
if 2nd male would fertilize eggs.
Mate guarding should pay off when females:
1. Scarce and hard to find.
2. Remain receptive after mating.
Example:
Clown shrimp.
Mate assistance hypothesis (MAH)
Male stays with partner because male
assistance increases young’s survival.
Increased survival of young outweighs
extra young gained by seeking extra mate
In seahorses, males
carry brood in pouch
during 3 week
“pregnancy.”
Pair stays together for
series of matings.
Male can hold only one clutch, so no benefit
in courting extra females.
Females choose monogamy because males
are scarce and because females are poor
swimmers and thus vulnerable to predators.
Female enforced monogamy hypothesis (FEMH)
In some species females actively prevent
males obtaining extra mates.
A female burying beetles will attack her mate if
he tries to release pheromones to attract other
females to a carcass the pair have buried.
In experiment, males whose female had been
tethered so she could not attack him
released pheromones for longer period than
males whose mate wasn’t tethered.
Monogamy in
birds
Male birds can feed young as well as females
(unlike most mammals).
Male assistance essential to rearing young.
Probably explains why > 90% of birds are
monogamous.
Male assistance in Snow Buntings essential
to rearing young.
Females whose males were removed reared
fewer than 3 young. Those with males reared
4 or more.
In many birds raising young so hard, it takes a
pair to rear even one young (e.g. albatrosses).
In Tree Swallows polygynous males father
fewer surviving young (0.8 fledglings)
than monogamous males (3.0 fledglings).
More offspring of polygynous males die
because male can’t help both females (MAH).
Females also mate with other males
because male cannot guard two females
effectively (MGH).
Monogamy best for both male and female
Tree Swallows.
Extra-pair copulations (EPC’s) in birds.
Even though monogamous males assist
one primary female, males also seek EPC’s.
DNA fingerprinting has shown EPC’s very
common.
DNA fingerprints
Right: Beta (**)
male unique band
occurs in
offspring
D, E, and F.
*
*
**
*
Above: * indicates
unique alpha bands
Alpha fathered all young.
Alpha male (*)
and offspring G
share unique band.
Male benefits of EPC’s are obvious
(increased offspring at low cost).
Why would females seek EPC’s?
Female may gain by :
1. Increasing chances of her eggs being
fertilized.
Female red-winged blackbirds who mate with
multiple males have higher egg hatching rates.
Similarly, female adders who mate with
multiple males have fewer stillborn young.
2. Obtaining better genes for her offspring
Many female Blue Tits mate with neighboring
males whose mates don’t seek out other males.
These males survive better and produce more
young than males with unfaithful mates.
Suggests they have better genes.
3. Obtaining resources from male
Female red-winged blackbirds that copulate
with neighboring males are allowed to forage
on the males territory.
Males RWB’s also assist in attacking predators
in vicinity of those females nests.
Polygamy
Any mating system involving mating with and,
in many cases, forming pair bonds with
multiple members of the opposite sex.
Three kinds:
Polygyny
Polyandry
Polygynandry
Polygyny: One male mates with two or
more females.
Examples : Birds: Lark Bunting, Red-winged
Blackbird, Dunnock, Marsh Wren.
Marsh Wren
Mammals: Lions, Gorillas, Bats.
Also found in many fish, insects, etc.
Three basic types of Polygyny
1. Resource defense Polygyny
2. Female defense Polygyny
3. Lek Polygyny
1. Resource defense polygyny.
Male defends resources that females need
to produce young (food, nesting sites).
Resource defense polygyny in an African cichlid
African cichlid fish Lamprologus callipterus
exhibits extreme sexual dimorphism
(males 13X times larger than females).
Females lay eggs inside empty snail shells and
remain inside shell until eggs hatch.
Males collect suitable shells and steal them
from other males.
Males gather shells into large collections and
defend them from rival males.
Up to 86 shells have been recorded in one
collection and up to 14 females at once.
Males with good territories obtain high
reproductive success.
Extremely large male body size has been
selected for because it enables males to collect
shells and to defend their territories.
Male Red-winged Blackbirds hold territory
on marshes. Males with the best territories
attract harems of up to 15 females.
Females choose males on the basis of
territory quality.
Male’s red epaulettes are
essential in male-male
competition.
Polygyny threshold model
Some females choose to mate with already
mated males who will not help them feed their
chicks even though unmated males with
territories are available.
Why would a female do this?
Polygyny threshold model: predicts that
female will accept role of 2nd mate (polygyny)
when superior resources on males territory
mean that female would do better there than
as 1st mate on a poor territory
Curves represent payoffs to female. Female
can choose between males A and B. A has
a mate, B is unmated.
Polygyny threshold model
Example of polygyny threshold.
Male Lark Buntings establish territories in
grassy, open habitats. Mate with > 1 female
but assist only first female to settle on their
territory.
Some female LB’s accept secondary female role
on good territory to obtain a high quality nesting
site.
In bad nest sites young die from exposure to
the sun.
Some male Pied Flycatchers establish two
territories. Sing to attract a female.
Males provide little help to female on 2nd
territory, so female has low reproductive
success.
Each female mated to a polygynous male has
lower reproductive success than a monogamous
female.
However, males r.s.
is higher than that
of a monogamous
male
Male Pied Flycatchers clearly try deceive
females into polygyny.
Not clear yet if females really fooled or have
no better alternative.
2. Female defense Polygyny.
Common when females cluster in groups that
are defensible.
Males then defend clusters against other males.
E.g. Elephant seals, lion prides, elk and deer
herds.
In some marine siphonoecetine amphipods,
which build protective cases out of gravel
and shells, males collect females and
glue their houses to their own.
In general, female defense polygyny possible
because females cluster for their own reasons
and males exploit this.
E.g. Lionesses cluster to defend feeding
territories.
Deer gather for protection.
Elephant seals gather on the few suitable
nursery beaches.
3. Lek Polygyny
Males do not help in raising the young.
Variance in male mating success is greatest
in this system.
Examples: Grouse,
Ruffs, manakins.
Cock-of-the-rock.
In lekking species males display for females
at a predictable location (a lek) and females
come to the site to choose mates.
Males provide no resources except sperm.
Males display for females. Females choose
males on basis of appearance and displays
(sexual selection).
Sage Grouse displaying on a lek.
Highly skewed mating success is normal in
lekking systems.
A few males obtain most of the matings.
By mating with best possible male,
females obtain the best available genes
for their offspring.
In well-studied Black Grouse and Sage
Grouse lekking systems < 10% of males
obtain 70-80% of the copulations.
Why do males gather in leks?
Gathering in leks may reduce predation risk.
Open country birds display in groups whereas
forest species usually display solitarily.
Birds-of-paradise that display in leks are edge
or second-growth species (where predation risk
is high) whereas primary forest species display
solitarily.
Three most favored hypotheses for
evolution of lekking are:
1.“Hot-spots” hypothesis
2. “Hot-shots” hypothesis
3. Female preference hypothesis.
Hot-spots Hypothesis: males gather at sites
where they are likely to encounter females.
Lekking bees, wasps and other insects often
use same locations for leks.
Territories of lekking flycatchers, manakins
and hummingbirds also often overlap.
Gather along streams or ridgelines that
act as highways for female movement.
Convergence of different species on same
location supports hot-spot hypothesis.
Hot-shots Hypothesis: subordinate males
cluster around most attractive males -“hot-shots” -- in order to be seen by or to
intercept females attracted to these males.
In Great Snipe (a bird) removing central
dominant bird caused neighbors to leave
territories.
Removal of subordinates resulted in their
territories being refilled.
In Black Grouse on long-lasting leks location
of most popular territory shifts from year
to year. Suggests male quality more important
than location in lek.
Female Preference Hypothesis: females prefer
to choose from groups of males because
comparisons are easier to make.
The mating behavior of the Ruff appears
consistent with all three hypotheses.
Male ruffs are named for their
well-developed ruffs, which they use to
display to females (reeves).
Ruffs are polymorphic with ruffs
occurring in a variety of colors.
Male ruffs use a variety of mating
strategies.
They pursue females (followers), wait for
them at rich feeding ground (interceptors)
or wait at classic leks (lekkers).
White-ruffed males appear to have evolved
as specialist Followers skilled at tracking the
movements of females between neighboring leks.
Male ruffs may switch tactics but
committed lekkers have the highest
mating success.
Dark morph ruff displaying to a female.
Controlled experiments suggest that female
ruffs prefer larger leks.
This preference increases the mating
success of males at large leks and favors
that breeding strategy.
Female ruffs prefer groups of at least five
males and visit such groups more often.
Leks with >5 males do not attract
more females, thus satellite males reduce
success of dominant males by intercepting
some of the females.
Hot-spots and hot-shots hypotheses also
relevant to ruff mating system.
Leks tend to be located by ponds where
females come to feed (Hot-spots).
Satellite males gather around most successful
males (Hot-shots).
The clustering of males on leks may in part be
due to a tendency of young or inexperienced
males to gather near older or successful males.
Such satellite males may get occasional
matings and perhaps gradually improve their
status.
Such associations are most extremely developed
in the Central and South American manakins.
Cooperative leks displays.
In many manakins males perform cooperative
displays. Three or four males may cooperate
to display but usually only the alpha male gets
to mate.
Round-tailed Manakin
Cooperative
display of
Swallow-tailed
Manakins.
In Long-tailed Mankin males may take 8 years
to move up to alpha position.
Four year study: in 117 observed copulations
only 8 of 85 males copulated.
90% of copulations by 4 males and 67% by one
alpha male.
Long-tailed Manakin
Manakin mating system works because
birds are long-lived and females tend to
return to where they mated before.
As a result, the beta and lower-ranking males
can expect to inherit a high-quality display
ground and can afford to delay mating.
Polyandry: One female forms pair bonds
with two or more males.
Female reproductive success is more variable
than male reproductive success in polyandrous
mating systems.
There are two forms: classic polyandry
and cooperative polyandry.
Classic Polyandry: Females lay clutches for
multiple males and compete for males.
Examples : Jacanas, Phalaropes, Spotted
Sandpiper.
Cooperative Polyandry: Two or more males
cooperate to assist a female at one nest.
Examples: Acorn Woodpeckers, Dunnock.
In classic polyandry females brightly
colored and compete for territories and males.
Males incubate eggs and care for young.
Female
Red
Phalarope.
Male Jacanas (lilytrotters) defend small
territories against other males.
Females defend larger territories that
include several male territories.
Female jacana lays clutch of eggs for each
male in her territory.
Male alone incubates eggs and cares for the
young.
Losses of eggs and chicks to predators and
nest flooding may be high.
Clutch of jacana eggs.
Male Pheasant-tailed Jacana incubating.
If female jacana loses her territory or dies
and another female takes over the territory,
the new female destroys the eggs and kills
young of any male on territory.
This behavior frees the male to incubate
a replacement clutch, which new female
provides.
Female Spotted Sandpipers are 25% larger
than males. Female will lay clutches for
a primary male and from 1-3 secondary males.
Only the last secondary male is assisted by
the female in caring for the young.
However, later males are likely to have lower
reproductive success because sperm from
earlier males may fertilize some of eggs.
Not clear how classic polyandry has evolved.
May be a result of heavy losses of eggs which
favor females maximizing egg output
(Jacanas).
Alternatively, in Spotted Sandpipers cause may
be phylogenetic constraints that limit females
to four egg clutches.
Females can produce more eggs because food
sources are rich, but must lay more clutches
not bigger ones. Hence, need males to
incubate.
Rare case of females being limited by access to
mates rather than by gamete production.
Cooperative Polyandry also occurs in which
more than one male assists a female.
Appears to be result of shortage of breeding
opportunities because there are few
territories available.
Groups of Acorn
Woodpeckers compete
for territories that
contain granary trees.
Cooperative Polyandry
may arise when a
multiple male coalition
controls a territory
with only one breeding
female.
In Dunnocks cooperative polyandry
occurs when two males partition a
females territory.
Polygynandry: Two or more females form
pair bonds with two or more males.
Examples : Ratites (i.e. Rheas and Ostriches),
Dunnocks, Acorn Woodpeckers.
Arises in similar circumstances to those just
described for Cooperative Polyandry.
The mating system of the Dunnock
“Unobtrusive, quiet and retiring, without being shy,
humble and homely in its deportment and habits,
sober and unpretending in its dress, while still neat
and graceful, the dunnock exhibits a pattern which
many of a higher grade might imitate, with
advantage to themselves and benefit to others through
an improved example.”
The Reverend F.O. Morris (1856) encouraging
his parishioners to emulate the humble life of the
Dunnock. Little did he know!
The Dunnock is an unobtrusive brown and gray bird
that is common in woodlands, hedgerows, and urban
areas in Europe.
The Dunnocks breeding in the Cambridge University
Botanical Gardens have been the subject of
long-term research by Nick Davies and colleagues.
These studies have revealed a mating system that
the Reverend Morris might have hesitated to
recommend to his parishioners.
Dunnocks feed on small arthropods and
establish and defend exclusive territories,
which they retain year-round.
Subject of long-term studies by Nick Davies
and colleagues in Cambridge University
Botanic Gardens
Females establish and defend their territories
against other females.
Females choose their nesting territories
independently of males and compete for
space with other females.
Territory size is a function of food
availability.
The more food is available the smaller
territories are.
Dunnock 1990 female territories
Male Dunnocks also defend territories but as
is the case for females, only against
members of their own sex.
Males impose themselves on the female
distribution and attempt to monopolize
access to the females territories.
Dunnock 1990 male territories
Female
territories 1990
Male
territories 1990
Monogamy arises when a male can control all of a
females territory.
In spring, males pursue females around their territories
thus learning the territory’s boundaries and singing to
stake their claim.
A male who can control a single territory is
monogamous. A male who can control more than one
territory is polygynous.
Polyandry usually arises when a
female’s territory lies between the
territories of two males.
Each male attempts to pursue the
female into the other males territory.
At first each male is dominant in its own
territory, but eventually one male (the alpha)
establishes dominance and the two males
(alpha and beta) defend the females territory
together.
Polyandry may also arise when a young male
persistently intrudes onto an older males
territory until he eventually is accepted as
a beta male.
Polygynandry may occur when in
adjacent monogamous pairs one male
invades the adjacent territory and
eventually becomes the alpha male in
a two female territory.
Female territory size is crucial in determining
the mating system.
The larger the female territories are the harder
it is for any mating system other than
monogamy or polyandry to arise because males
cannot defend very large territories.
Territory size is a function of food availability.
The more food available the smaller female
territories are.
If food is added, female territory size is reduced
and this facilitates polygyny and polygynandry
Males are larger than females and dominant over
them in aggressive interactions. When food
is scarce, females lose out to males.
female


As a result of male dominance, female mortality
is higher in severe winters.
As a consequence of differential mortality the
population sex-ratio is male-biased after severe
winters.
A shortage of females leads to an increase in
polyandry.
Males and females both try to maximize their
reproductive output.
Male and female payoffs differ in different
mating systems.
Payoffs
For male
For female
Polyandry
Share one
female
Sole access
to multiple males
Monogamy
Sole access to
one female
Sole access to
one male
Polygynandry
Share several
females
Share several
males
Polygyny
Sole access to Share one male
several females
When more than one male feeds a brood
more young are fledged and they are bigger.
The larger young are at fledging the better
their chance of surviving to independence.
A male’s payoff is highest when he can
mate with multiple females.
A female’s reproductive success is highest
when she can obtain the assistance of more
than one male to care for her brood.
These aims are in opposition in polyandrous
and polygynandrous mating systems.
In a polyandrous or polygynandrous
mating system a female dunnock tries to
encourage both males to feed the young.
She does this by mating with both males
and giving them paternity in the brood.
The alpha male, however, wishes to control
mating access to the female because although
more young are reared when both males feed
the brood, the number of young he fathers
is reduced.
Male Dunnocks try to maximize their reproductive
success by engaging in sperm competition
and mate guarding.
Sperm Competition
In Dunnocks sperm competition is
intense.
Male Dunnocks produce > 1000 times
the amount of sperm that the comparably
sized Zebra Finch does.
Females store sperm in special sperm
storage glands.
Sperm Competition
Both males mate with the female as often as they
can to maximize the amount of their sperm in the
female’s sperm storage glands.
Both males also engage in cloacal pecking. In this
behavior the male before mating pecks the females
cloaca and she ejects stored sperm from her sperm
storage glands.
Mate Guarding
The alpha male guards the female and tries to
prevent her from mating with the beta male.
If the beta male attempts to mate, the alpha male
intervenes and drives him away from the female.
The female encourages the beta male to
mate and attempts to escape from the alpha male
and mate with the beta male.

Mate Guarding

The alpha male
intervenes in
copulation attempts
made by the beta male.


Both males frequently inspect the nest to
see if eggs have been laid and value copulations
during the egg-laying period particularly highly
as these are most likely to produce offspring.
After the eggs have been hatched beta males base
their decision on whether to feed the brood
or not on the amount of mating access they have
had to the female.
The greater the mating access a beta male has had
the more often he feeds the young.
DNA fingerprinting results have been very
useful in teasing apart the mating success
of males and females in these complex
mating systems.
Right: Beta (**)
male unique band
occurs in
offspring
D, E, and F.
*
*
**
*
Above: * indicates
unique alpha bands
Alpha fathered all young.
Alpha male (*)
and offspring G
share unique band.
The Dunnock’s mating system results from the
interaction of multiple factors both ecological and
behavioral.
Food supplies and winter conditions affect female
territory size which determines how many female
territories a male can defend.
This in turn leads to complex behavioral maneuvering
as both sexes attempt to maximize their reproductive
success.
Hardly, the picture of domestic tranquility that the
Reverend Morris had in mind!