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Mating systems, sociality and mate choice in animals: contributions of molecular ecology

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Title: Mating systems, sociality and mate choice in animals: contributions of molecular ecology


1
Mating systems, sociality and mate choice in
animals contributions of molecular ecology
2
Mating Systems and Sexual Selection
  • Diversity of mating systems
  • Polyandry, Polygyny, Polygynandry, and Monogamy
  • Consequences male-male competition, female
    choice
  • Honest signals, good genes
  • Runaway selection, exaggerated characters,
    linkage of genes for female preference with genes
    for male traits

3
Mating Systems and Sexual Selection
  • Polyandry
  • One female, several males
  • Male jacanas (Microparra spp.) do most nest
    building
  • After the female has laid a clutch of four eggs,
    the male takes over the parenting
    responsibilities
  • Jacana nests are built on mostly submerged
    plants. If the nest starts to sink, the male
    carries to a new site
  • Meanwhile, the female has left the male to find
    more males to breed with
  • She does not participate in raising chicks
  • If the eggs or chicks are lost, she will return
    to breed and produce a replacement clutch with
    the first male

4
Mating Systems and Sexual Selection
  • Polygyny
  • One male, several females
  • Much male-male competition. Males compete for
    females by defending important resources (like
    foraging grounds in blackbirds) or by attracting
    females to display grounds (like grouse leks)
  • In birds, some males defend female harems
  • Montezuma oropendola
  • Males defend colonies of females, alpha male
    rules (like elephant seal) and gets most of
    copulations (and pass on most genes)
  • Females do all the nestling care
  • Clue to occurrence is sexual dimorphism (larger
    males) and grouping behavior of females

5
  • In a Costa Rica population of this bird,
    high-ranking males defended groups of females at
    nesting colonies
  • Alpha vs. beta vs. low-ranking males
  • DNA fingerprinting assessed paternity

6
Apparent alpha (RRR) and beta (OMO) male mating
success (based upon behavior observation)
7
Analysis of DNA fingerprint data
  • Jeffreys 33.15 probe, and M13 probe
  • Multilocus band patterns on gels
  • Band sharing S2n/T
  • N bands shared
  • Ttotal bands in both lanes
  • Within group relatedness r(Sw-Sb)/(1-Sb)
  • Sw band sharing within groups
  • Sb band sharing between groups
  • Group colony presumably governed by one male

8
Distribution of band sharing
  • A between adults
  • B between adult females and nestlings
  • C between adult males and nestlings this
    indicates that 11 nestlings could be assigned
    paternity

9
Revelations due to fingerprinting
  • Paternity was examined for 21 nestlings from four
    colony sites.
  • Seven nestlings matched with the alpha male at
    their colony, 4 matched with the beta male, and
    10 did not match any sampled male.
  • Fertilization success of alpha males was
    significantly lower than expected from the
    observed copulations
  • Paternity assignment and levels of band sharing
    among nestlings indicate that most nestlings not
    attributable to the alpha were sired by several
    low-ranking males copulating away from the
    colony.

10
Within group relatedness
r(Sw-Sb)/(1-Sb)
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Mating system of sea lions
  • Pinnipeds often show unconventional and
    sneaky mating tactics to increase their
    reproductive success, and these can be less easy
    to observe.
  • Males tend to control a harem (Harem holders)
  • They sometimes control more than one harem at the
    same time, or switch between being the holder of
    one harem and the peripheral of another harem.
  • Use DNA to discover the true pattern of mating
    success!

13
of harem progeny sired by harem holder
brackets are number of progeny sired by harem
holder
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Issues in this study
  • Compares reproductive patterns with size of
    population
  • But power of paternity inference decreases with
    population size

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18
Mating Systems and Sexual Selection
  • Polygynandry
  • multiple males and females
  • Smiths Longspur
  • Females pair and copulate with more than one male
    for a single clutch of eggs
  • Males pair and copulate with two or more females
  • Intense sperm competition due to promiscuous
    females
  • Several males routinely feed a single brood
  • All males in a neighborhood sing SAME song
  • Allows males to easily recognize intruders and
    females to mate only with local males who will
    help her raise brood

Briskie 1999
19
  • Paternity analysis
  • digest DNA with MboI or Alu1
  • Run on gel, probe with one of several probes
    (per, Jeffreys, 33.15, 33.6 and lambda)

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Monogamy
  • Common Crossbill (Kleven et al. 2008)
  • Many passerines seem to have mates for life
  • However extra-pair paternity may be common in
    socially monogamous passerines

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Monogamy
  • Common Crossbill (Kleven et al. 2008)
  • no evidence of extrapair paternity among 96
    offspring in 34 examined broods.
  • Common Crossbills thus seem to represent an
    exception to the rule of extrapair mating among
    socially monogamous passerine bird species.
  • A potentially important selective pressure
    preventing promiscuity
  • in Common Crossbills is the harsh environmental
    conditions experienced during breeding at
    wintertime, which may increase the importance of
    paternal care and limit the time available for
    seeking extrapair copulations.

27
Tradeoffs
  • Migration may limit resources (energy and time)
    available for investment in parental care and
    territory defense
  • Sexual selection for parental care may reduce
    time and energy available for migration
  • Breeding systems may determine or respond to
    migration behavior

Shorebirds Garcia-Pena et al. 2009)
28
Costs of breeding systems
More malemale competition leads to increased
bias toward male mortality Female-female
competition does not
Parental care also is costly
Liker and Szekely 2005
29
Conservation implications
  • Polygyny can be costly
  • In sage-grouse modelling study Ne was only 19 of
    N because of variation in reproductive success
    between years and the skew in breeding sex ratio
  • Resulted in small effective population (42) which
    may suffer inbreeding effects (low hatchability
    was observed
  • Need to manage for larger than one might expect
    population sizes

(Stiver et al. 2008)
30
Conservation implications
  • Flexible mating systems may counteract
    synchronized environmental fluctuations
  • When sex ratio becomes skewed, if polygamy can
    occur, then chance of extinction is reduced
  • Lesser Spotted Woodpecker in Germany
  • Models suggest that when male skew in sex ratio
    occurs, then polyandry would reduce probability
    of extinction

(Rossmanith et al. 2006)
31
Optimal Group Size
  • Sociality can reduce individual workload, fear,
    predation, finding unpredictable foods, etc
  • Sociality can increase disease, competition,
    conspicuousness, cuckoldry
  • Tradeoffs can give optimal size
  • Kin selection theory may explain evolution of
    groups

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Raven Information Centers
  • (1) Roosts comprised both knowledgeable and naive
    foragers.
  • (2) Departures from roosts were highly
    synchronized, with most members departing in one
    direction.
  • (3) Direction of departure often changed from day
    to day.
  • (4) Birds made naive of food sources (by being
    withheld from the wild and then allowed to join
    roosts) followed roost-mates to new feeding
    sites, whereas control birds held and released
    outside of roosts rarely found the local food
    bonanzas.
  • (5) Birds made knowledgeable of food sources (by
    being released at new carcasses) joined roosts
    and led roost-mates to the food on three of 20
    occasions.
  • (6) The same individuals switched leader and
    follower roles depending upon their knowledge of
    feeding opportunities.

(Marzluff et al. 1996)
34
Why do groups form?
Not Kin Selection
Parker et al. 1994
35
Animal mating systems viewpoint of a
quantitative geneticist (Stevan J. Arnold)
36
Qualitative classification of mating systems
  • Monogamy, polygamy, polyandry (Darwin 1871)
  • Monogamy, resource defense polygyny, harem
    defense polygyny, explosive mating assemblage,
    leks, female access polyandry (since Darwin)

37
Limitations of qualitative classifications
  • Progeny can be produced by matings that are
    difficult to observe.
  • Difficult to specify how the categories grade
    into one another.
  • Essential differences may masquerade under the
    same name.
  • For all these reasons, we need quantitative
    characterizations.

38
Determination vs characterization of mating
systems
Spatial distribution of resources
Operational Sex ratio
Variation in reproductive success
Intensity of sexual selection
System of mating
Emlen Oring 1977
39
Fundamental information about the mating system
is captured in the parental table
Arnold Duvall 1994
40
Selection theory measures
  • Quantify Batemans three principles (variance in
    mating success, variance in offspring number,
    relationship between offspring number and mating
    success)
  • Standardized variances, regression slopes
  • Direct connection to theory for selection on
    quantitative traits
  • Is, Is I, I ßss, ßss

Bateman 1948, Crow 1958, Wade 1979, Wade
Arnold 1980, Arnold Duvall 1994, Shuster
Wade 2003
41
The relationship between ßss, Is, and I
ßssslope 1.46 offspring/mate
I0.18
Is0.21
42
Properties of a selection opportunity, I
  • Equals variance in relative fitness
  • Sets upper limit on the magnitude of directional,
    stabilizing (disruptive), and correlational
    selection
  • When this variance is zero, there can be no
    sexual selection

43
Properties of a Bateman gradient
  • Equals the slope of the regression that relates
    reproductive success (offspring) to mating
    success (mates that bear progeny)
  • Part of the selection that acts on every
    sexually-selected trait
  • The final common path between sexually-selected
    traits and fitness
  • When this gradient is zero, there can be no
    sexual selection

Arnold Duvall 1994
44
The relationship between ßss, Is, and I
ßssslope 1.46 offspring/mate
I0.18
Is0.21
45
A parental table and Bateman plots derived from
it
46
The Bateman gradient as a part of selection on a
trait
Arnold Duvall 1994
47
Same thing with plant mating systems, but with
inbreeding
48
Parental table and Bateman plots for a population
with partial selfing
49
Theoretical perspective connections to
evolutionary theory
Inbreeding coefficient
Selfing rate
Inbreeding depression
Selection on selfing rate
Inheritance
Evolution of selfing rate
Lande Schemske 1985
50
Summary of insights from the empirical perspective
DATA EVOLUTIONARY PARAMETERS THAT CAN BE ESTIMATED
Mating success Opportunity for sexual selection
Reproductive success Opportunity for fecundity selection, Bateman gradients
Traits in males and females Sexual and fecundity selection gradients
Traits in offspring Heritabilities (G-matrix), response to selection
Fitness of offspring Heritability of mating and reproductive success, parental selection
Inbreeding coefficients or pedigree Inbreeding depression, coefficients of inbreeding
51
Summary
  • Characterization of mating systems using
    selection and inbreeding theory measures has
    advantages over other characterizations.
  • The parental table offers a useful empirical
    perspective on mating systems, and can be
    inferred via paternity analysis.
  • In some mating systems and for some purposes, the
    parental table needs to be supplemented with
    additional information (e.g., parental traits,
    offspring fitness).

52
MHC and Mate Choice
  • MHC evolution and how we select a mate

53
  • Among the constellation of genes that control
    the immune system are those known as the major
    histocompatibility complex (MHC), which influence
    tissue rejection.

Conceive a child with a person whose MHC is too
similar to your own, and the risk increases that
the womb will expel the fetus.
If the smell of MHC isn't a deal maker or
breaker, the taste is. Saliva also contains the
compound, a fact that Haselton believes may
partly explain the custom of kissing,
particularly those protracted sessions that stop
short of intercourse. "Kissing," she says simply,
"might be a taste test." (Kluger, 2008)
54
Why Sex?
  • Considered the deepest mystery in all of
    biology. (Trivers, 1985)

55
Red Queen hypothesis about parasite resistance
  • New combinations of genes for resistance are
    required in every generation to cope with the
    currently dominating parasites.

It takes all the running you can do, to keep in
the same place. (Carroll, 1872)
56
Major histocompatibility complex (MHC)
  • 1940 Discovered in mice in connection with skin
    grafting
  • Name refers to the region of several linked genes
    that controls skin grafting
  • Connection to immune system not determined until
    1960s/70s

Abbas and Lichtman, 2005
57
Abbas and Lichtman, 2005
58
MHC Genes
Abbas and Lichtman, 2005
  • Human MHC molecules are called Human Leukocyte
    Antigens (HLA)
  • Most polymorphic genes in genome
  • Codominantly expressed
  • Categorized as Class I or Class II

59
Three requirements for MHC to be a basis of mate
choice
  • Females must
  • Know there is an enormous variation in resistance
    genes in the population
  • Know her immune genes
  • Recognize the immune genes of potential mates and
    choose

60
The infamous T-Shirt test
  • Males and Females were typed for HLA- A, -B, and
    -DR
  • Males wore shirts for two consecutive nights
  • Women rated smell of shirts on pleasantness,
    intensity, and memory association
  • Two sample populations
  • Oral contraceptive users
  • Non-oral contraceptive users

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Results
63
Red Queen is still a hypothesis
  • Need evidence showing selection for rare MHC
    alleles, in response to the ever-changing
    parasite load
  • This would the mechanism that maintains MHC
    polymorphism

64
Mate choice motives to choose different MHC
genotype
  • Reduce inbreeding?
  • Specific MHC selection?
  • Increase MHC heterozygosity?
  • Maximize diversity across several loci?
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