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

Mating systems, sociality and mate choice in animals: contributions of molecular ecology. Mating Systems and Sexual Selection. Diversity of mating systems Polyandry, Polygyny, Polygynandry, and Monogamy Consequences: male-male competition, female choice Honest signals, good genes

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

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  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 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)

  11. 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!

  12. % of harem progeny sired by harem holder brackets are number of progeny sired by harem holder

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

  14. 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

  15. 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)

  16. 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

  17. 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.

  18. 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)

  19. 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

  20. 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)

  21. 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)

  22. 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

  23. 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)

  24. Why do groups form? Not Kin Selection Parker et al. 1994

  25. Animal mating systems:viewpoint of a quantitative geneticist (Stevan J. Arnold)

  26. 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)

  27. 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.

  28. Temporal availability of the limiting sex 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

  29. Fundamental information about the mating system is captured in the parental table Arnold & Duvall 1994

  30. 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 Bateman 1948, Crow 1958, Wade 1979, Wade & Arnold 1980, Arnold & Duvall 1994, Shuster & Wade 2003

  31. The relationship between βss, Is, and I βss=slope= 1.46 offspring/mate I=0.18 Is=0.21

  32. 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

  33. 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

  34. The relationship between βss, Is, and I βss=slope= 1.46 offspring/mate I=0.18 Is=0.21

  35. A parental table and Bateman plots derived from it

  36. The Bateman gradient as a part of selection on a trait Arnold & Duvall 1994

  37. Same thing with plant mating systems, but with inbreeding

  38. Parental table and Bateman plots for a population with partial selfing

  39. Theoretical perspective: connections to evolutionary theory Inbreeding coefficient Selfing rate Inbreeding depression Selection on selfing rate Inheritance Evolution of selfing rate Lande & Schemske 1985

  40. Summary of insights from the empirical perspective

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