Ethology &
Behavioural Ecology
The Evolution of
Reproductive Behaviour
Chapter 10 Alcock (Animal Behavior)
Tom Wenseleers
Plan of talk
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Evolutionary origins of two sexes
Typical sex roles
Reversed sex roles
Male-male competition
Female choice
Aims & Objectives
• Aims
– Present a simple model for the evolution of male
(small gamete) and female (large gamete) roles.
– How sex differences in parental investment select for
typical sex roles (e.g. choosy females) + exceptions
• Objectives
– Learn examples
– Understand the evolutionary logic in the evolution of
gamete size differences and typical sex roles
1. Evolutionary origin of two sexes:
small gametes (males)
& large gametes (females)
NOT IN TEXTBOOK!!
Origin of gamete size differences
Will the mutant producing smaller gametes be selected for? Model Maynard Smith
Assume small gametes are half size and that the mutant can make twice as many as a
result.
Yes
If survival of smaller embryo is >50% that of normal embryo
No
If survival of smaller embryo is <50% that of normal embryo
Note that small embryo is 75% the size of the large embryo, and that when rare (i.e. new
mutant) small gametes only fuse with large gametes. We are only considering "invasion"
conditions, meaning a rare small gamete mutant in a population making large gametes.
Graphical model
The curve represents the survival of the immature individual as a function of the size of
the embryo resulting from the fusion of two gametes in an ancestral situation when
gametes were of one size.
Graphical model
The tangent from the origin shows the size of the embryo,a, that maximises survival per
unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is
the values on the survival curve).
Graphical model
The tangent from the origin shows the size of the embryo,a, that maximises survival per
unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is
the values on the survival curve).
Graphical model
The optimal size of a gamete is half of the optimal size of an embryo.
Graphical model
Would making half sized gametes be favoured? Yes. A half size gamete fusing with a
normal gamete results in an embryo 75% the normal size with survival b. And making
twice as many half size gametes gives more surviving offspring since 2.b > a.
Conclusion
• The model in the previous slides presents the idea that
from an initial situation of equal-sized gametes, it is
possible for smaller gametes to be at an advantage. In
other words for two sexes to evolve in a sexually
reproducing population in which there is initially only one
sex.
• However, the advantage of the smaller gametes will
decrease as they get more common if fusion is at
random. E.g., if two small gametes would fuse the
embryo might be too small to survive. We might expect
small gametes to evolve the ability to avoid fusing with
each other. This would cause the evolution of two distinct
mating types, males and females.
2. The evolution of
typical sex roles
Typical sex roles
Angus Bateman & Robert Trivers: typical male and female
sex roles come about because of sex differences in
investment in individual offspring.
MALES
invest little in each offspring
can potentially have large numbers of offspring
can greatly increase fitness by having multiple partners
rarely can increase fitness by being choosy
FEMALES
invest a lot (more than males) in each offspring
cannot, potentially, have large numbers of offspring
cannot greatly increase fitness by having multiple partners
usually can increase fitness by being choosy
Angus John Bateman
Robert Trivers
Males: typically brightly coloured
male
as a result of female choice
males are usually more
brightly coloured to attract
females
female
gang gang cockatoo
Males: typically larger
male
female
orangutan
as a result of male-male
competition males are
usually larger and
stronger than
females
Eager males and choosy females
# fertilisable females < sexually active males
(♂-biased operational sex-ratio)
selects for “eager” males and “choosy” females
males should frequently want to mate with
females when they don’t want to
females should be choosy and reject lowquality males
Coercive sex
Not enforced
Long courtship
Enforced
No courtship
Struggle
Iron cross blister beetle
Traumatic insemination
spermalege
Male bedbugs have a saber-like penis that they insert
directly into the abdomen of their mates prior to
injecting them with sperm. Such traumatic insemination
may have evolved to overcome female choosiness.
Female counterdefence: spermalege (modified region
of abdomen where male pierces female).
A counteradaptation to
male sexual exploitation
simulated penis
with sterile needle
simulated penis
with dirty needle
Another female counterdefence
Dunnocks (heggemus):
females eject sperm of
low-status males
Davies Nature 1983
Females: typically more choosy
Clark & Hatfield J. Psych. Hum. Sex. 1989
Males
“Would you go to bed with me tonight?”
“Would you go out with me tonight?”
Females
Females: typically more choosy
Clark & Hatfield J. Psych. Hum. Sex. 1989
“Would you go to bed with me tonight?”
“Would you go out with me tonight?”
Males
75%
50%
Females
0%
56%
But sex roles still much more equal in humans than in any other primate,
because of the large contribution of males in the upbringing of children.
Test: sex role reversal
• How can we test Trivers' idea that typical sex roles
come about because of sex differences in
investment in individual offspring? For example, that
females are more choosy than males because they
invest more in the offspring, and so are limited in the
number of offspring by how much they can invest.
• We predict that there will be sex role reversal in
those species where males invest a lot in offspring.
For example, because the male provides a costly
nuptial gift to the female, or provides costly parental
care to young.
Pipefish: males that get pregnant
Hippocampus: brood in pouch
Syngnathus: brood in pouch
Phyllopteryx: brood on tail
Sex role reversal in pipefish
• Males get "pregnant" and provide oxygen and nutrients
to a clutch of eggs held in an egg pouch
• During the time of male pregnancy females of some
species (e.g. Syngnathus scovelli) can produce enough
eggs to fill 2 male pouches.
• Given an even sex ratio, male pouch space is therefore
in short supply.
• Males in these species tend to be sex role reversed, and
tend to be choosy (they select females which provide the
most eggs)
• However in other genera, e.g. Hippocampus, the female
egg laying rate is limiting. In these there is no sex role
reversal.
Sex role reversal in pipefish
Nutritious spermatophores
In many insects, the male transfers nutrients with his sperm or provides a resource for
the female to eat when mating ("nuptial gift"). This has been much studied in Orthoptera
(crickets, grasshoppers).
Sex role reversal in Katydids
A female of the Australian Katydid Kawanaphila eats a spermatophore whilst sitting on a
pollen-poor kangaroo paw flower.
Sex role reversal in Katydids
If the difficulty of making nuptial gifts changes, then this
may change choosiness. Males should be more choosy
when the resources needed to make the nuptial gift are
scarce.
This was tested in the Australian Katydid Kawanaphila.
Food supply varies greatly through the breeding season.
When food is limited to pollen-poor kangaroo paw flowers
spermatophores are hard to produce, and so very valuable.
The males are often choosy and the females compete for
males.
But when food is abundant males rarely are choosy and
females do not compete for males.
Sex role reversal in Katydids
Male Katydids provide a large nuptial gift at mating. Males are
choosy when the resources (pollen) needed to make the gift are
scarce.
Sex role reversal
in mormon crickets
Mormon crickets are large, flightless Orthoptera. Males transfer an enormous edible
spermatophore to females when they mate as a nuptial gift. Constitutes 25% of a male's
body mass.
Sex role reversal
in mormon crickets
Males transfer an enormous edible spermatophore to females
when they mate as a nuptial gift. This constitutes 25% of male's
body mass. Males probably can mate only once.
Females can produce several egg clutches, provided that they
can persuade several males to mate with them.
Males put more resources in, so the operational sex ratio is
female biased. That is, there are more females looking for males
than vice versa.
High densities of mormon crickets can form. When this happens,
males stridulate. Females come quickly to the male, and jostle to
compete for chances to mate with him.
Males exercise choice over which females to mate with,
preferring larger females who will be more fecund. That is a male
chooses a female who will be able to lay more eggs fertilised by
his sperm.
Sex role reversal
in mormon crickets
Sex role reversal
in mormon crickets
Being choosy is beneficial for males of the mormon cricket (USA). They mate
with larger, more fecund, females.
Sex role reversal:
the wattled jacana
Male uniparental care
Causes male to carry most of
the cost of offspring production
Results in choosy males and
ornamental, eager females
Most birds have biparental
care, and these do not show
sex role reversal
Emlen et al. 1998
Conflict over sex roles in
hermaphrodites: flatworms
both want to become the male
(minimum investment)
"penis fencing": first one who is
stabbed by the other’s penis
becomes the female and has to
produce expensive eggs
Pseudobiceros hancockanus
Michiels, N.K., and L.J. Newman. 1998. Sex and violence in hermaphrodites. Nature 391(Feb. 12):647
Conflict over sex roles in
hermaphrodites: banana slug
penis chewing: the one whose
penis is bitten off first becomes
the female
can take 12 hours
A.B. Harper 1988, B.L. Miller 2005
Banana slug
Sexual selection
• Charles Darwin: made a distinction between
natural selection (acts on individual survival) and
sexual selection (acts on likelihood to mate)
• intrasexual selection: competition within one sex
for mating opportunities, e.g. male-male fights
• intersexual selection: likelihood to mate affected
by interactions between the two sexes, e.g. as a
result of female choice
Male ornaments
selected due to female choice
intersexual competition
Antlers
male-male competition
intrasexual competition
European stag
red
beetle
deer
quetzal
peacock
red deer
3. Male-male
competition
Male-male competition
• Male-male competition manifests itself in a wide
variety of adaptations on the part of males, many
of which have a strong behavioural component.
• Fighting and selection for large body size
Alternative mating tactics
alternatives that are equally rewarding
alternatives not equally rewarding
(best of a bad job)
Mate guarding
Sperm competition
etc... etc...
Fighting
Developmental costs
Males of the dung beetle fight for mates. Beetles with long horns (left) have a
fighting advantage but tissue that goes into horn construction (blue) is
unavailable for the building of eyes (yellow). As a result, males with long horns
(left) have smaller eyes than rivals with short horns (right). Both types may well
be equally fit.
Body size and mating systems in seals
In seals, there is strong correlation between sexual dimorphism and polygyny.
The sexes are of similar size in species where males cannot monopolise a
large number of females. Where males can monopolise a harem of females,
there is an advantage to large male size and this results in greater size
dimorphism.
Body size and mating systems in seals
Elephant seal males can
weigh 2000 kg. They fight
vigorously and dangerously.
The winner (beachmaster)
commands a harem of
dozens of females.
The other males skulk away
and get few or no matings.
But maybe in a future year
one of them will be the
beachmaster.
We can show that fighting is to acquire mates by correlating male
dominance with mating success.
Body size and mating systems in seals
McCann's work on southern elephant seals on South Georgia.
Recent DNA analysis shows that mating success is tightly linked
with paternity.
Sexual dimorphism
Big elephant seals can win fights with other males and thereby get
high reproductive success by monopolizing a lot of females. There
is therefore tremendous selection pressure on elephant seal males
to get large.
But it takes a lot of time and energy to get big. We can predict that
costly investment in the growth and maintenance of large bodies will
only occur when exceptional rewards are accrued by large
individuals.
Also, there will come a point where there is no longer any individual
advantage of growing larger or being more fierce (recall the hawkdove game).
Where mating occurs is also very important. If males cannot access
and monopolise many females then extreme dimorphism should not
occur. E.g., if mating occurs in the ocean vs. on the beach.
Dominance correlates with
reproductive success
In Savanna baboons in Kenya
there was a strong correlation
between male dominance rank
and the ability to monopolize
fertile females across all
groups studies.
Alternative mating tactics
Alternative male morphs in an isopod
(fighter)
(female mimic)
(hider)
The isopod Paracerceis sculpta lives
inside sponges in the Gulf of
California. Males occur in three
distinct morphs each with a different
genotype. Each morph has equal
fitness, and has different advantages
in terms of mating. The alpha morph
can physically fight off other males.
But in a sponge with several females,
an alpha male and a beta (female
mimic) male, it is the female mimic
who fathers the most offspring. Thus
the advantage to female mimics
increases if the alphas become more
common. Natural selection results in
the three morphs occurring at
frequencies at which their fitness is
equal.
Alternative male tactics in lizards
side-blotched lizard (Uta stansburiana)
Lizards play rock-scissors-paper
Alternative male tactics in scorpion flies
Scorpion flies are not flies but
insects in the order Mecoptera.
The male genitalia vaguely look
like a scorpion tail, hence the
name.
There is at least one common
species in Belgium (Panorpa
communis) which can often be
seen in hedges and tall vegetation
looking for prey.
Alternative male tactics in scorpion flies
Alternative strategies: unequal fitness
Scorpion flies (Panorpa):
10 males and 10 females in a cage
Large males
guard dead insects attractive to
females; N=6 matings each
Medium-sized males
produce salivary gifts to attract
females; N=2 matings each
Small males
force copulations on females
N=1 mating each
Males adopt different mating
tactics depending upon size.
The largest guard dead
insects who are attractive to
females. Smaller males use
other tactics, such as
producing nuptial gifts. But if
the large males are removed
smaller males will adopt the
large male tactics. Faced with
competition from larger males
the smaller males adopt
tactics which reflect their poor
competitive ability. This is
known as making the "best of
a bad job".
Three male strategies
Isopods
equal fitness
frequency dependent equilibrium
Lizards
not equal fitness; cyclical dynamics
blue beats orange
yellow beats blue
orange beats yellow
not equal fitness; best of bad job strategy
large male: guard insect
medium male: salivary gift
small male: forced copulation
Scorpion flies
Making the best of a bad job
In the horseshoe crab males in good condition patrol the water off the
beach and find and grasp females heading towards the shore to lay their
eggs. Other males (satellite males) in bad condition swim onto the
beach alone and crowd around paired couples to try to fertilise some
eggs. Attached males fertilise 10 percent more eggs than satellite
males, but satellite males still do better than if they would try to attach
themselves to a female and be displaced by stronger males.
Coalition formation
A significant number of
subordinate baboon males
are able to get access to
estrous females by forming
coalitions with other lowranking males. Again, they are
making the best of a bad job.
Iguana's
Small, subordinate iguana males can win out from larger ones by
ejaculating beforehand and keeping the sperm up to the brief moment
they get a chance to mate, and before they are driven off by larger
males.
Sperm competition
Sperm competition
male-male competition can continue after
sperm is released in both internally and
externally fertilising species:
sperm competition
Sperm competition in damselflies
male
male sperm transfer organ
claspers
female
Calopteryx maculata: black-winged damselfly (N-America)
Female may mate with several males. But male has a special penis that can
draw out sperm from other males that mated with the female before, and this is
90-100% effective. But: female could choose to mate with yet another male.
Sperm competition in damselflies
Calopteryx maculata: black-winged damselfly (N-America)
Male penis has lateral horns which act as a brush and draw out sperm from
other males.
Bean beetle males
harm females
Crudgington & Siva-Jothy Nature 2000
Bean beetle males harm females during insemination
with a specially adapted spikey penis. This prevents the
female from mating with another male.
Seminal toxins in the fruit fly
Male injects female with
toxin (protein ACp62F)
Sedates female and
prevents her from mating
with other males
But costly to female:
shortens her lifespan
Chapman et al. Nature 1995
Seminal toxins in the fruit fly
Holland & Rice: made a
selection experiment.
They bred males and
females forcing them to
be either monogamous or
polygynous. The males
from the monogamous
lineage showed reduced
expression of the seminal
toxins and the females
also partly lost their
immunity to the toxin.
Mate guarding
Mate guarding
male damselfly graps the female in
the tandem position so she cannot
mate with another male
male blueband goby accompanies
female for his whole life
Mate guarding in the Seychelles warbler
Clutch size = 1 egg; male guards
fertile female; guarding ends when
egg laid; fake egg can switch off
male's guarding early.
Seychelles warblers lay a single
eggs. When this is laid the male
need no longer guard his mate
against rivals. By placing a fake
eggs in the nest c. 4 days before
the female laid the real egg, the
experimenters were able to switch
off guarding. The result is a
massive increase in the number of
intrusions, attempted an
successful EPCs (extra pair
copulations) by males.
Mate guarding in the Seychelles warbler
Males adjust their mate guarding in relation to the risk of losing
paternity to rivals. The more male neighbors around a breeding pair
the more time male warblers spend guarding their partner.
Mate guarding in blue milkweed beetle
Does time spent guarding your
partner against other males give
more offspring than abandoning her
and looking for more mates?
Janis Dickinson investigated this in
the blue milkweed beetle. The male
remains mounted on female's back
for some time after copulation.
Mate guarding in blue milkweed beetle
Dickinson removed male beetles from females.
25% of separated males found a new mate within 30 minutes. So
guarding the female has a considerable cost in terms of missed
mating opportunities.
50% of females found a new mate after guarding male was removed.
So guarding the female has a considerable benefit in preventing the
female from remating.
Where do the costs and benefits balance out? By plugging these and
other factors into a simple model it appears that guarding is beneficial
if the last male fathers 40% or more of the female's offspring.
Can you understand why this is so? If the last male fathers less
offspring, then this means the female is less worth guarding (you
were the last but probably not the only male to mate her), and if
another male mates her he won't father many of her offspring
anyway.
4. Female choice
Female choice to obtain
direct material benefits
• female choice most common
• several mechanisms, e.g.
– accepting sperm of males with large nuptial
gifts
– rejecting sperm from low status males
– remating or not
– also: pollen incompatibility in plants - reject
own pollen
• usually gives direct material benefits
Accepting sperm of males with large
nuptial gifts: hanging scorpionflies
Females copulate with a male for as long as they can keep on feeding on
the nuptial gift. If this takes less than 5 minutes no sperm is transferred; 20
mins is required for complete transfer.
Remating or not in redback spiders
Male transfers sperm and then commits
suicide by jumping into the jaws of the
female who then usually eats the male.
This may seem maladaptive, but it is not:
feeding the female by committing suicide
reduces the chances that the female will
mate with and dine on another male. Also,
chances for a male to find another female
are very slim because of intense predation.
The selective pressure caused by females
who may are may not remate has led to the
evolution of male suicide.
Sperm ejection in Chickens
Female chickens who have mated with a low status male are
more likely to eject the sperm from their reproductive tract.
Sperm ejection in Dunnocks
Dunnocks (heggemus): male may peck at partner's cloaca if
another male has been near her. In response she may eject a
droplet of fluid containing sperm.
Female choice for males that
provide more care
Females of the fifteen-spined stickleback associate more with males
that shake their bodies more frequently, which is a good indicator of
how well they will be able to oxygenate the eggs later on.
Female choice for males that
provide more care
Sedge warbler (rietzanger): male song repertoire indicative of how good a father they
will be later on. Females prefer to mate with males with a bigger song repertoire.
Female choice without
direct material benefits
• previous examples: consistent with good
parent theory
• but also in species without paternal care
females often prefer distinct males, e.g.
with brightly coloured plumage
• why?
Healthy mate theory: bowerbirds
Male bowerbirds with high-quality bowers are less likely to carry ectoparasites in their
feathers, so females that copulate with good bower builders will be less likely to pick
up feather lice.
Good genes theory:
sedge warblers
Sedge warbler males: repertoire size is correlated with male heterozygosity. Females
prefer males with a large repertoire and therefore also more outbred males. This
increases the heterozygosity, and genetic quality, of the female's offspring.
Good genes theory:
starlings
Starlings (spreeuwen): males that sing at a higher rate have a stronger immune
response measured by the swelling of a foreign chemical into their wings. Since
females prefer males with high song rates they could be acquiring mates with strong
immune systems, which will also be passed on to their offspring.
Good genes theory:
Hamilton & Zuk hypothesis
Hamilton & Zuk: in species subject to parasitic infection,
individuals that can signal their relatively parasite-free state
should be desirable males. They further argued that only high
quality, parasite-free males would be able to produce costly,
bright plumage displays (cf. Zahavian handicap). This would lead
to plumage coloration being an honest signal of the male's ability
to resist parasitic infections.
Supportive evidence: correlation between plumage brightness
and the incidence of blood parasites across a large sample of
birds.
Good genes theory:
peacock
Male peacocks with larger eye-spots on their
tails produce offspring that survive better when
released from captivity.
Runaway selection theory
Genes responsible for the male display have a pleiotropic effect
when present in females and causes them to prefer males
producing the display. Also has the advantage that the males that
a female produces will also be preferred by females ("sexy
sons").
Could work even if it causes females to prefer purely arbitrary
characters with no survival advantage, or even a survival
disadvantage.
Russell Lande & Mark Kirkpatrick
A preexisting sensory bias
Male and female guppies eat Clusia fruits which are orange due to
the presence of carotenoids. The same carotenoids also accumulate
in males and lead to colourful patterns.
Observation: females prefer colourful males.
Why? Preexisting sensory bias for detecting orange fruits.