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 probe, and M13 probe
Multilocus band patterns on gels
Band sharing S=2n/T
N=# bands shared
T=total # 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)

12. 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

15. Issues in this study
Compares reproductive patterns with size of population
But power of paternity inference decreases with population size

18. Mating Systems and Sexual Selection
Polygynandry
multiple males and females
Smith’s 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)

24. 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

26. 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 male:male 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

33. 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)
Newts and violets

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)
Many proposed schemes from Darwin’s time to the present … Useful but leave many aspects of the mating system in doubt

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.
The effort to find quantitative characterizations of mating systems has several motivations …

38. Determination vs characterization of mating systems
Temporal availability of the limiting sex
Spatial distribution of resources
Operational
Sex ratio
The distinction between determination and characterization can be illustrated with this diagrammatic portrayal of Emlen & Oring’s (1977) scheme. Variables that determine the mating system (input) are shown in black; variables that characterize the mating system (output) are shown in green. One goal since 1977 has been to define the variables in green and specify with equations the relationships among them and to the determination variables.
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
All three categories can be calculated from the parental table; what is it? … Will use the parental table to take an empirical perspective on the characterization problem. Two issues: (1) Do the measures capture all the info in the table? (2) Is all the necessary information in this table?
Arnold & Duvall 1994

40. Selection theory measures
Quantify Bateman’s 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; βss, βss
Selection theory measures have a long history streching back to 1948…
Bateman 1948, Crow 1958, Wade 1979, Wade & Arnold 1980,
Arnold & Duvall 1994, Shuster & Wade 2003

41. The relationship between βss, Is, and I
βss=slope= 1.46 offspring/mate
I=0.18
The Bateman gradient is the regression slope in a plot that relates reproductive success to mating success. The two selection opportunities are the standardized variances of the two marginal distributions.
Is=0.21

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
In addition, the gradient gives the magnitude and direction of selection for multiple mating
Arnold & Duvall 1994

44. The relationship between βss, Is, and I
βss=slope= 1.46 offspring/mate
I=0.18
The Bateman gradient is the regression slope in a plot that relates reproductive success to mating success. The two selection opportunities are the standardized variances of the two marginal distributions.
Is=0.21

45. A parental table and Bateman plots derived from it
There are two Bateman gradients, one for each sex. In many polygynous mating systems, males have a steeper Bateman gradient than females (as in this example; and as has beenshown in newts). In polyandrous mating systems, we expect females to have a steeper Bateman gradient (as in pipefish).

46. The Bateman gradient as a part of selection on a trait
One of the key properties of a Bateman gradient is that it represents part of the selection that acts on all sexually-selected traits. This property can be seen in this path diagram, which shows how fitness is determined by a hierarchy of variables …
Arnold & Duvall 1994

47. Same thing with plant mating systems, but with inbreeding
On their way to the breeding pond, nexts often walk over violets in bloom. Students of mating systems of violets and other plants are obsessed with inbreeding. … Chasmogamy and cleistogamy in violets … inbred and outcrossed progeny

48. Parental table and Bateman plots for a population with partial selfing
In the parental table for a population with partial selfing, two kinds of progeny are produced … inbred (yellow) and outbred (blue) … Notice that row and column lables refer to the same individual parent … inbreeding depression can not be estimated from the data in this table … we need a estimate of offspring fitness for each blue and yellow cell … More generally, we also need a inbreeding coefficient for each cell.

49. Theoretical perspective: connections to evolutionary theory
Inbreeding coefficient
Selfing rate
Inbreeding depression
Selection on
selfing rate
Inheritance
This diagram portrays the theoretical perspective on a mating system with partial selfing. Variables that characterize the mating system are shown in green. Relationships supported by equations are shown as solid arrows….
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 evolution and how we select a mate
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.
Article published in Time magazine that looked at The Science of Romance published Jan 28, 2008.
A proposed mechanism of how MHC selection occurs follows.
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. You have 2 mice, one has an A allele the other B
You take a skin graft from both and transplant to type A mice
Type A accepts, Type B rejects
Immunization: This shows illustrates how not all MCH respond to the same protein anitgen.
When injected type A showed response, type B did not.
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
Located on Chromosome 6
At some HLA loci more than 250 alleles
You express both your mother’s and your father’s allele--->more molecules to bind peptide for presentation

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
To ensure “natural odor” men were given perfume free soap and detergent. Also asked to refrain from use of deordorants, colognes, refrain from smoking, drink alcohol and to sleep alone in bed.

62. Results
Non-contraceptive users: Found the scent of males with MHC-dissimilar to their own to be more pleasant, whereas females who used contraceptives found MHC-similar males more pleasant
MHC-dissimilar males more frequently reminded the women of current mate/ex-mate
Couples who had successive failed IVF were found to have a significantly greater number of related HLA antigens than those who achieved pregnancy via IVF

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
Simply put…a rise in Parasite 1 should show a rise in Allele Y, that combats Parasite 1, in the following generation.

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