Mating Systems in Sexual Animals

Mating systems reflect natural selection on mate choice and strategies for maximizing individual
reproductive success
Animals evolve species-typical strategies for maximizing reproductive success
o Results in a lot of diversity in mating patterns
Evolution of Sex
Cost of sex: pass on half as many genes to offspring compared to asexual animals
Sex is more common than asexual reproduction due to evolutionary advantages
o Genetic recombination offspring will be more genetically diverse
Advantageous for local environmental changes
Eg. Aphids reproduce asexually in stable environments and sexually
when environment turns cold since sexual eggs are freeze tolerant and
can diapause (suspend development)
Evolved defenses against parasites and disease
Eg. Mud snail host to several trematode parasites sexual individuals
more common in high risk of infection areas and asexual more common
in low risk of infection areas
o Increase chance of acquiring favorable mutations
o Unlikely propagation of deleterious mutations
Due to differential gamete investment among sexes, females may spend more care than males
during mate selection (high cost)
Variance in Mating Success and Batemans Principle
Batemans principle variance among females in mating success is low, and high in males
o One mating in females could fertilize all eggs but male reproductive success is based on
number of times mated
o I.e. nearly all females in a population mate and have offspring but relative few males
mate successfully
Males that do mate tend to have many partners, thus few males have very high
reproductive output and many males have little or no reproductive output
Sexual selection should act more strongly on males, resulting in greater
elaboration of behavior and structures used for attraction
o Criticisms focus on generality of predictions
Multiple matings of females could be advantageous
Eg. Female cichlid fish mates with any male because high risk of
predation and small population ensures chance of offspring
Eg. Female Malawi blue cichlid has high population but multiple mating
could avoid inbreeding, increase genetic diversity, increase likelihood of
compatible mate (not sterile and help prevent infanticide)
Female Mate Choice
Females are choosier, mostly because of higher investment in gametes
Choose males for good genes (predictors for better survivorship of offspring), good potential
parenting, possession of resources to support offspring during growth and development
Females more likely to provide parental care
Selection favors females that choose males that enhance likelihood of offsprings success
Mating is a costly and females may be choosier due to risks aggression, disease transmission
Male Mate Choice
Importance of male mate choice is controversial
o Older theory predicts male mate choice should be less common

o Important in many mating systems

o Cost of male mating underestimated in earlier studies
Occurs most often when males substantially involved in caring for offspring, or when theres
great variation in quality of females in population
If males are choosy, over time females may evolve ornamentation or coloration subjecti to sexual
selection
Types of Mating Systems
Monogamy
o Social monogamy single male with single female
Most common in birds, rare in other animals
Both sexes will contribute to defense and parental care of offspring
Inappropriate mate has high fitness cost
o Serial monogamy (extra-pair copulations)
Can develop if cost of poor mate is very high
Very common in birds
Higher genetic variation among offspring
Benefits of monogamy (shared parental care and territorial resources) maintained
by having one mate at a time or concealing extra-pair partnerships
Polygyny one male with multiple females
Most common in mammals, found in few birds and insects
Male strategy to increase reproductive fitness
o Resource Defense Polygyny groups of females attracted to a resource and males
compete for territorial possession and thereby mating priority
o Harems defended group of females associated with one male
Females may initially associate for group defense or herded together by male
Males compete for control of group
Dominance hierarchy among females of group
Leks aggregation of males seeking to attract mate
o Males perform sexual displays
o Near attractive females or where females likely to travel
o Not associated with resources
o Attract more females than individual males strategy to increase reproductive success
Polyandry one female with many males
Helps female ensure reproductive success by having multiple mating options
o Resource Defense Polyandry females control resources, which controls male mating
associations (Spotted Sandpiper)
o Cooperative Polyandry all males in group copulate with female and all participate in
brood provisioning (Galapagos hawk)
Polygynandry multiple females and males mate with each other, and males amy care for broods
of several females
o Groups can live together and less concerned with mate competition
o Advantageous for female paternity confusion which decreases infanticide and multiple
males care for brood
o Chimpanzees and bonobos
Promiscuity no pair bonds, males and males mate randomly (sometimes choosy)
o May occur in unpredictable environments

Sperm Competition (not mating system) male-male competition, males sperm must be first to
reach egg
o External fertilization in aquatic animals, animal that releases largest amount of sperm
and sperm that is highly capable of swimming will produce most offspring
o Internal fertilization physical removal of sperm
Sexual Selection
How Sexual Selection Came To Be Recognized
Sexual selection is composed of intersexual selection (competition between same sex for access
to mates, usually males) and intersexual selection (one sex choses members of opposite sex,
usually females)
Theory of female mate choice was ridiculed and not seriously considered until 80 years later
Which Sex is Under Stronger Selection?
Sex roles are defined by differences in gametes
Asymmetry leads to Batemans principle, female reproduction limited by access to resources and
male reproduction limited by access to females
Sexually reproducing species average reproductive success is equal between sexes since every
offspring has mother and father
Successful male can take away opportunities from other males, leading to high reproductive
variance among males
Successful female does not take opportunities from other females, leading to small variance in
reproductive success
Higher reproductive variance, stronger effects of sexual selection
o Strong sexual selection leads to exaggerated sexually dimorphic traits in sex with highest
reproductive variance
The Role of Parental Care
Most species provide little or no care to offspring
In species requiring parental care, variance in reproductive success impacted by fertilization
success and contribution of each sex to care of offspring
Degree and direction of sexual dimorphism can be explained by relative selection gradients of
each sex
o If females provide more care, variance in male reproductive success is large since
females will not be immediately available for further reproduction and competition for
available females will increase
o In biparental care, variance in male reproductive success is lower, since males that
provide care will not invest much energy in pursuing more mates =. Leads to sexually
monomorphic species
o If males provide more care, males become limiting resource for females, thus variance in
productive success is high for females who then tend to monopolize access to one or
more males => reversed sexual dimorphism, females more elaborate secondary sexual
characters
Choosing A Mate
Females can directly increase reproductive success by mating with certain males and acquiring
benefits
o Direct benefits: increased access to food, protection from harassing males, help in raising
offspring, avoid being infected with parasites and diseases
o Indirect benefits: genetic rather than resource based, offspring inherit genes that increase
fitness

Males evolve traits that display ability to provide benefits and females evolve preferences for
these traits
Good Genes variation in males gives information about genetic quality that can be inherited by
offspring
o Lack of evidence for this model
Fisherian Arbitrary Choice female preference can evolve for arbitrary traits that do not provide
information about male quality, and thus do not reinforce the effects of natural selection
o If females prefer a trait, males with that trait will be selected upon, and the fitness
advantage of this trait exists as a result of its covariance with the preference
o Females gain indirect benefit of offspring that are more sexually attractive to females
with that preference
When Does Sexual Selection Act?
Affects reproduction success at multiple reproductive stages
o Acts during all processes that lead to acquiring mating opportunities (pre-copulatory)
o Post-copulatory events that occur after mating
Sperm competition
Post-copulatory female choice ability of females to affect likelihood that sperm
fertilizes eggs and decision to invest in offspring based on identify of male whom
they mate
Morphological, chemical, and behavioral adaptations
Conflict Between the Sexes
Traits that increase male reproductive success at expense of female will be selected if female
mates with multiple males and reproductive success of these males is higher than males lacking
trait
Sexual conflict can result in evolutionary arms race: evolution of trait imposes harm on one sex
leads to counter-trait to mitigate harm on affected sex with subsequent escalation in both
o Eg. Traumatic insemination in bed bugs, copulatory grasping and anti-grasping structures
in waterstriders, and genital coevolution in waterfowl
Cooperation, Conflict and the Evolution of Complex Animal Societies
The Costs and Benefits of Group Living
Before joining group, individual must weigh cost-benefits
o Benefits: more eyes to look for predators or help forage, assistance in dealing with
pathogens (grooming), easier mating opportunities, conservation of heat, reduced
energetic costs of movements
o Costs: groups are more conspicuous to predators, increased competition for food and
reproduction, increased parasite burden, misdirected parental care
Many species form short-term, unstable groups: wildebeest, gulls
Some form long-term, stable social groups, with altruistic interactions
o In repeated interactions, there is incentive for altruistic behavior
Kin Selection and Living in Families
Altruistic behavior can benefit individuals even if not reciprocated
o William Hamilton extent an individual is willing to help another is determined by
degree of relatedness due to sharing of genes
Evolutionary fitness is determined by fraction of individuals genes that enter
next generation, regardless of whether gene comes from that individual or
identical copies in relatives

Organisms can enhance direct fitness by reproducing or indirect fitness by

helping relatives
Hamiltons Rule - rB > C, calculates percentage of genes shared between two
individuals to determine costs and benefits of cooperative ac
Termed kin selection John Maynard Smith
Eusociality in Insect Societies
Eusocial (truly social):
1. Cooperative care of young
2. Overlapping generations
3. Reproductive division of labor, often culminating in caste development
First formally described in ants by Wheeler most notable in bees, wasps, and termites
Successful coordination relies upon the majority of group members forgoing personal
reproduction
o Workers specialize on tasks, extraordinary efficiencies of scale
o Helping behavior in insects is a product of both coercion and voluntary actions
Coercion in honeybees, individuals cant choose reproductive role and develop
into either workers or queens based on nutrients received in larval stage
Voluntary in honeybees, individuals maximize fitness by rearing relatives
Worker honeybees unable to mate, but can lay unfertilized eggs that become
male
Rarely occurs when queen is alive because workers police other
workers, destroying eggs
o Maximizes fitness of police workers by ensuring energy is
devoted to raising daughters of queen (sisters) and not nieces
Cooperative Breeding in Vertebrate Societies
Alexander Skutch made first observations of cooperative breeding in birds
Cooperative groups have breeders and non-breeding helpers which raise offspring of others
Unlike insects, vertebrate helpers are totipotent (can give rise to complete embryo) and retain
ability to reproduce throughout life
In most cooperatively breeding species, helpers tend to be related to breeders and therefore
realize indirect fitness benefits of raising relatives
Group sizes much smaller in vertebrates than insects
Common in birds and mammals
Kin selection cannot entirely explain why some species are social and some are not
o Environment influences species sociality
If individual is low in resources, may be better to help family raise relatives than
breeding unsuccessfully
Hostile and unpredictable climates cooperative breeding is a conservative
strategy when breeding conditions cannot be accurately predicted year to year
Best of a bad job strategy

Ten Sinister Parasites that Control Their Hosts Minds

Zombie ant fungus (Ophiocordyceps unilateralis)
Spore infects ant foraging on rainforest floor, spends 3-9 days developing inside its body
Manipulates ant to go ~25 cm up a tree, right amount of humidity for fungus growth
Ant clamps down on leaf with mandibles and dies

Within 24 hours, fungal threads emerge from corpse, stalk pushes out of ant and rains spores onto
rainforest floor to infect more ants
Kamikaze horsehair worm (Paragordius tricuspidatus)
Horsehair worm larva eaten by larva of another insect, mosquito or mayfly
Once emerges from water, cricket or grasshopper eats it and horsehair worms develops inside
Worm alters functions of crickets central nervous system and coerces it to jumping into body of
water
Cricket drowns itself and horsehair worm emerges
Castrator barnacles (Sacculina sp.)
Barnacle enters crab through chink in claw joints, sheds hard shell to squeeze in
Leeches crabs nutrients and turns crab into reproductive vehicle
If crab is female, barnacle forces it to care for millions of barnacle larvae
If crab is male, it is feminized to do same thing
o Becomes infertile, grows larger abdomen to carry barancles young, gonads shrink, and
stops developing fighting claws
Green-banded broodsac (Leucochloridium paradoxum)
Flatworm goes into stalks of snail, looks like caterpillars to entice birds
Manipulates snail behavior snail positioned themselves to more exposed, better-lit places,
higher up in vetgtation
Once eaten by bird, worm can reproduce
Ladybird parasite (Dinocampus coccinellae)
Wasp stings ladybird, leaving behind an egg
Egg hatches, larva chews through ladybirds internal tissues and bursts through abdomen to spin
cocoon between its legs
Ladybird becomes bodyguard over cocoon, thrash and twitch limbs if predator approaches (may
be due to venom of larva)
Emerald cockroach wasp (Ampulex compressa)
Wasp delivers paralyzing string, hijacks roachs mind, injecting an elixir of neurotransmitters into
its brain
Recharges of roach blood, chews off its antennae, and leads to nest
Lays eggs in roachs abdomen, and barricades it in with pebbles
Wasp larva eats roach alive, and adult bursts out of remains
Toxoplasmosis (Toxoplasma gondii)
Single celled, mainly infects rats and mice in order to be eaten by a cat for reproduction
Infected rats and mice lose fear of smell of cats, and become attracted to a pheromone in cats
urine
o Less likely to hide under floorboards and more likely to sniff around feline predators
Affects 30-60% people, unusually common in people with schizophrenia
Rabies viruses
Spread through saliva, usually from scratch or bite
Host becomes more aggressive, compelling it to spread virus through biting and scratching
Influenza virus
Makes people more sociable, those given flu vaccine interacted with significantly more people, in
larger groups in 48 hrs after exposure than 48 hrs before
Schistocephalus solidus
Hafer and Millinski infected copepods with multiple tapeworms which need to move onto fish
host, stickleback

Tapeworms manipulate copepods to be more active and thus more likely to be spotted and eaten
If two tapeworms were both ready to move hosts, effect on copepods behavior was even stronger
suggesting cooperation
If older tapeworm and younger tapeworm, host copepod still active suggesting older tapeworm
was sabotaging younger competitor

Evolution and the Origins of Disease

Darwinian medicine studying medical problems in an evolutionary context
o Asks why the body is designed in a way that makes us vulnerable to problems, offering
broader context to conduct research
Bodys flaws fall into few categories
o Evolved defenses
Coughing to clear foreign matter, those who do not are likely to die from
pneumonia
Those that cannot feel pain usually die by early adulthood from tissue damage
and infections
Fever facilitates destruction of pathogens elderly rates that cannot achieve high
fevers like young counterparts move to hotter environments when have infection
Low levels of iron in blood iron is sequestered in liver to prevent invading
bacteria to get adequate supplies of the vital element
Morning sickness coincides with period of rapid tissue differentiation in fetus,
when most vulnerable to toxins nauseated women restrict intake of potentially
harmful substances => women with more nausea less likely to suffer
miscarriages
We can harm ourselves by using drugs which block our defenses
False alarms like vomiting when no toxin is present only cost a few calories
but missing a real alarm may be death
Natural selection favors the smoke detector principle human has numerous
smoke alarms, regulation mechanisms with hair triggers
Explains why blocking defenses is often free of tragic consequences
since most defensive reactions are to insignificant threats
o Conflicts with Other Organisms
Natural selection cant protect us from all pathogens since they tend to evolve at
a faster rate
Our defenses are potent selection forces
Pathogens quickly evolve counter defense or become extinct
Pathogens can seemingly adapt to every chemical researchers develop
Conflicts can occur within species too, eg. Mother and her fetus optimal size of
fetus is smaller for mother than it is for fetus and father
o Coping with Novelty
Heart attacks only became widespread in this century and is rare among huntergatherers
Poor decisions about diet and exercise made by brains shaped by environment
substantially different from now fat, salt, and sugar used to be scare and
individuals that had tendency to consume large amounts had selective advantage
Substances such as nicotine, cocaine, and opium are productions of natural
selection to protect plants from insects

Humans share common evolutionary heritage with insects and thus many
of these substances affect our nervous system
Breast cancer more prevalent in modern society, and most cases are not solely
genetically based may be due to having more menstrual cycles, larger time
between menarche and pregnancy
Trade-offs and Constraints
o Genes that cause diseases must have other benefits, in some environments, or would not
be so common
eg. Sickle cell anemia
o Aging is ultimate example of genetic trade-off
Genes that cause aging and death could be selected for if they had advantageous
effects in youth, when force of selection is tronger
Pleiotropic genes genes with multiple effects
Possible that genes that cause aging have no benefit at any age but never
decreased reproductive fitness enough to be selected against
Evolution of Darwinian Medicine
o Darwinian approach makes sense only when object of explanation is changed from
diseases to the traits that make us vulnerable to diseases
o Incorrect assumption that natural selection maximizes health selection maximizes
reproductive success of genes
Genes that make bodies having superior reproductive success will be more
common even if it compromises individuals health

Ecology and Evolution of the Flu

Flu is unusual because the primary timescales for disease dynamics (epidemics) and viral
evolution (new variants) are roughly the same
Annual flu epidemics important cause of mortality, particularly to elderly and those with chronic
diseases
o Severe flu pandemics can threaten healthy individuals too
What is the flu?
Flu is a respiratory infection in mammals and birds
o RNA virus Orhtomyxoviridae family
o Three main types: A, B, C distinguished by two major internal proteins
o Flu A is most important and interesting because its found in wide variety of birds and
mammals, can undergo major shifts in immunological properties
Divided into subtypes based on differences in membrane proteins hemagglutinin
(HA) and neuraminidase (NA)
Most important targets for immune system
Currently two types in humans: H1N1 and H3N2
o Flu B mostly confined to humans
o Little known about C, not important source of morbidity (relative incidence of disease)
Little is known about transmission of flu importance of airborne transmission relative to droplet
transmission is controversial
Recovery from flu is believed to grant lifelong immunity to closely related strains
o Evidence: 1977 re-emergence of H1N1, after being absent from 1957-1977, infected
mostly people under 20 since older individuals retained immunity
The burden of flu

WHO estimates respiratory infections killed >4 million people in 1999 => most dangerous
category of infectious disease
o Flu contributes to many of these deaths but difficult to say how many
Since flu kills mostly elderly, there is a lower loss of total life years than would be expected by
high mortality estimates
Flu ecology
Flu coexisted with humans for >400 years
Incidence data for flu generally not available since theres no reporting requirement for flu in
most countries, and its easily confused for other respiratory infections, but there is some data:
1. Monthly records of mortality attributed to pneumonia and influenza
2. Weekly records of influenza-like illness on a five-point scale
3. Weekly laboratory-confirmed cases of flu by type
Flu epidemics in Northern and Southern hemispheres are ~6 months apart
o Suggests climatic influence on flu transmission
o Influence of timing of school terms
Flu evolution
Flu is unusual because it continuously undergoes immunologically significant evolution
o Infection gives lasting immunity but most people are susceptible to new circulating strain
within a few years
Flu A and B show drift evolution: high rate of viable, immunologically significant mutations
o Can drift away from recognition by immune system by changing properties of antigenic
sites so cant be recognized, particularly HA protein
o Patterns of change suggest evolutionary modifications of antigen properties occur rapidly
o Sites involved in antigen determination: nucleotide substitutions that change amino acid
are more frequent than synonymous substitutions
Rest of sites show the more common pattern of synonymous variation
o Evolution of flu seems to be strongly influenced by selection for new antigenic variants
to escape immune system recognition
Recent developments in molecular biology and computation have made remarkable phylogenetic
reconstructions of flu evolution possible sequence data publically available
o H3N2 subtype: evolution seems to follow a single track over long term, at every
branching point a branch is destined for extinction
o Flu A: significant drift evolution takes around a year
A, but not B, undergoes dramatic antigenic changes known as antigenic shifts
caused by reassortment between different strains of flu within single host
Shifts probably result from segments of viruses circulating human
population and segments from avian viruses
Avian flu viruses can infect humans without passage through an
intermediate host and without acquiring gene segments from human flu
viruses
Interventions
Vaccine was first tested in 1935-1936, two years after virus was first isolated from humans, and
recommended for general use in early 1960s
Viruses evolve quickly so new vaccine must be designed every year
In most of world, vaccine uses trivalent inactive vaccine (TIV) cultured in chicken eggs
o Composed of B, A subtype H1N1, and A subtype H3N2
Efficacy of flu vaccines depends critically on individuals vaccination and infection history
because antibodies from previous exposures can inhibit effect of current vaccines

Modeling flu
Mathematical modeling has contributed significantly to understanding infectious diseases
Viral and bacterial respiratory infections: domination epidemiological modeling framework is the
box model host population is divided into compartments according to infection status
Childhood diseases: standard susceptible-infectious-recovered (SIR) model
Flu requires a more complex model due to antigenic drift
o Strains usually divided into variants which are immunologically distinct
o Susceptibility to variant will depend on persons history of infection with all variants of
given subtype
o To capture complete immunological histories for a model with n variants of one subtype,
would have to divide population into more than 2^n compartments
Simplifying model:
o Andreasen et al. use models where variants constrained to evolve along straight-line path
to estimate drift rates
o Gupta e al. use simple allele structure and assume that cross-immunity affects only
transmission and not infection
Few attempts have been made to model spatial spread of flu
The Evolution of Aging
Aging is an Evolutionary Paradox
Senescence inevitable progressive deterioration of physiological function with increasing age,
demographically characterized by an age-dependent increase in mortality and decline and
fecundity
Evolutionary explanation for aging requires explanation that is based on individual fitness and
selection, not group selection
Haldane, Medawar, and Williams realized that aging does not evolve for good of the species
but because natural selection becomes inefficient at maintain function and fitness at old age
o Mathematically formalized by Hamilton and Charlesworth
The Force of Selection Declines with Age
Force of atural selection, a measure of how effectively selection acts on fecundity (survival rate),
declines with age
Haldane proposed that declining strength of selection with age might explain relatively high
prevalence of domination allele causing Huntingtons disease
o Since Huntingtons mostly affects people >30 years old, would not be efficiently
eliminated by selection in ancestral, pre-modern populations since most people would die
before
Medawar:
1. For most organisms, world is dangerous so in natural populations most individuals die or
get killed before they can grow old and suffer symptoms of aging => individuals have a
small probability of being alive and reproductive at advanced age
2. Strength of NS declines with increasing age such that selection ignores performance of
individuals late in life => selection is unable to favor beneficial effects, or counteract
deleterious effects, when they are expressed at late age
a. If effect happens past reproductive age, it will not affect fitness
b. Even if mutation occurs earlier, its effects may not be visible if environmentally
imposed mortality is high and individuals that could express mutation are likely
dead
The Mutation Accumulation Hypothesis

Medawar reasoned that if effects of deleterious mutations were restricted to late ages, carriers of
negative mutation would have already been passed on to next generation
o NS would be weak and inefficient at eliminating mutation, and over evolutionary time
mutations would accumulate in population by genetic drift => evolution of aging
o Medawars mutation accumulation (MA) hypothesis
o Effects of mutation accumulation would only manifest at organismal level after
environment changes and individuals experience less extrinsic mortality and live to old
age
MA hypothesis was put on firm mathematical group by Charlesowrth
The Antagonistic Pleiotropy Hypothesis
Williams took Medawars ideas step further, argued that mutations or alleles that have opposite,
pleiotropic, effects at different ages might exist
o Genetic variants that are beneficial early in life, when selection is strong, but are
deleterious when selection is weak
o Known as antagonistic pleiotropy (AP) hypothesis for evolution of aging
o If beneficial effects outweigh deleterious effects such genetic variants would be favored
and enriched in population, leading to evolution of aging
o Evolution of aging can be seen as a maladaptive byproduct of selection for survival and
reproduction during youth
o Early fitness components (such as reproduction) should trade-off with late fitness
components (survival at old age) so that genotypes with high early fecundity should be
shorter lived than those with low reproduction
Similar to Kirkworks disposable soma (DS) hypothesis optimal level of
investment into somatic maintenance and repair will evolve to be below that
required for indefinite survival
Evolution of a higher investment unlikely to pay off due to extrinsic
mortality
Investment into reproduction might withdraw limited resources that
could be used for somatic maintenance and repair
Evolution of Lifespan
Organisms vary dramatically in lifespan
Independent of aging, reproductive lifespan can evolve adaptively in response to selection for
reproductive success
o Low adult mortality, high juvenile mortality, and high variation in juvenile mortality from
one reproductive event to next=> lengthen reproductive lifespan
Evolution of lifespan is a balance between selection for increased reproductive success and
factors that increase intrinsic age-dependent components of mortality
Semelparous organisms reproduce once and then die
Williams: only organisms with a separation of germ line and soma should age => germ line
maintained indefinitely, but aging soma is disposable after reproducing
o However, bacteria do not exhibit clear distinction between germ and soma and do not
have clear age classes (divide symmetrically) so should be immortal
o But symmetrically dividing E. coli ages, has subcellular mother-offspring asymmetry
Ackermann et al. modeled origin of aging in history of life and found that even when cells divide
symmetrically, unicellular evolve state of asymmetric, unequal distribution of cellular damage
among daughter cells
As soon as asymmetry evolves, aging evolves
Aging might be a fundamental property of cellular life