Mammals that feed their embryos by a placenta present an

1. Chase-away selection: genomic imprinting Mammals that feed their embryos by a placenta present an opportunity for males to fight females after mating has occurred Male strategy: force female to invest all of her energy into his offspring (immediate payoff) Female strategy: save energy for future clutches of offspring (save for the future) Genes involved in growth of the fetus are imprinted differently in males and female gametes

2. Chase-away selection: genomic imprinting Imprinted genes are differentially methylated, to turn expression on or off in the zygote (which grows into a fetus) Insulin-like growth factor II gene (IGF-II) promotes cell growth IGF-II is switched off on maternal chromosome, but on the paternal chromosome this gene is switched on - daddy forces mommy to invest more energy in fetal growth An unrelated receptor (CI-MPR) is switched on on the maternal chromosome, but is turned off on the paternal chromosome - binds excess IGF-II before it can trigger fetal growth - allows mother to slow fetal growth

3. Chase-away selection: genomic imprinting IGF - paternal imprinting: accelerate fetal growth mpr paternal maternal - maternal imprinting: slow fetal growth MPR igf note: these are not different alleles; they are differences in the way genes are expressed, due to methylation patterns that are laid down in testes and ovaries

4. Sexual antagonism depends on mating system (Holland & Rice, 1999) The previous experiment looked at fly populations where mating occurred among large groups, and promiscuity was common - male exploitation of females quickly evolved when there there were opportunities for multiple sex partners New experiment: What happens when flies are forced to pair up and be monogamous (one partner for life)? monogamy treatment: one female housed with one male control: one female housed with three males (multiple mating opportunities, as commonly occurs in nature)

5. Effects of monogamy after 34 generations (1) females reproduced more, but also survived more (2) males attempted fewer matings

6. Effects of monogamy after 47 generations reproductive rate - Monogamy increased the overall reproductive rate for the population - Also increased the development rate of offspring - Monogamous populations became better adapted development time of offspring generation 45 46 47

7. Effects of monogamy Monogamy constrains the reproductive success of both mates to be identical - neither sex can exploit the other when there’s no one else to mate with Former conflicts between mates turn into opportunities for mutualism (i.e., everybody-wins scenarios) - Males evolved to be less harmful to females - Females evolved to be less resistant to male-induced harm Mating fidelity (=cooperation) removed the costs of antagonistic coevolution between the sexes

8. Effects of monogamy In bat species where females are promiscuous (mate with multiple males), males evolved larger testicles(advantage in sperm competition) - monogamous species: testes up to 1.4% of male body weight - promiscuous species: testes up to 8.5% of male body weight but advantage in sperm competition comes at a price: males of promiscuous species also have smaller brains Promiscuous species: male body uses more energy to enhance testes -- trade-off: lack energy to further develop the brain In species where females are faithful to one partner, males have smaller testes and bigger brains Pitnick et al. 2006, Proc Roy Soc B

9. Why Cheat? If promiscuity leads to evolutionary conflicts between males and females that drags down everyone’s fitness, why don’t all species evolve to be monogamous? Advantages of promiscuity are clear for males - allele coding for a trait that gives one male an advantage in mating may “invade” a population & spread quickly - once it fixes, however, such an allele may drag down the average fitness of all individuals - examples: - behaviors that predisposes cheating - structures that give a mating advantage

10. close-up of stylet For instance, some hermaphrodites mate by hypodermic insemination – injecting sperm directly into any individual’s body The sharp penial stylet is an example of a trait that initially confers a mating advantage on any male that inherits it SEM courtesy of Sandra Millen

11. 1st slug to carry a mutation producing a primitive stylet will have a huge advantage at fertilizing many mates Allele will quickly rise in frequency in the population, as stylet-bearing slugs out-reproduce regular slugs However, once everyone has a stylet, all slugs also get injected, which can hurt SEM courtesy of Sandra Millen

12. Why do females cheat ? Male promiscuity is easily understood: maximize quantity But even in “monogamous” species, femalepromiscuity turns out to be common  in over 70% of bird species, females cheat on their partner  in many species, 20-50% of clutches have more than one biological father (but only one male raises the chicks) - up to 85% cheating in Superb Fairy Wren (M. cyaneus) - only 9% cheating in Shag (P. aristotelis), ironically Polyandry is the term for mating with multiple males

13. in Panama, the giant false limpet S. gigas forms mated pairs on rocks...

14. Why do females cheat ? Female promiscuity is thought to maximize the genetic quality(or maybe the variability) of offspring, in case... a) your mate is just kind of a loser (sleep around = better chance to find a superior male) b) your mate is not a good genetic match for you, specifically (for instance, he carries the same recessive allele as you) c) full siblings (similar) compete for the same resources; (cheating = some offspring are half-siblings, less similar) d) the environment changes: multiple mates = variable kids, greater chance at least some will survive new conditions

15. Benefits of polyandry I: Genetic compatibility Lifetime benefits of polyandry demonstrated in crickets: 1) females that mated with multiple maleshad higher success rates for egg hatching, even if they mated fewer times overall 2) no male was a consistently better father, in terms of offspring hatching success; success depended on which female they mated with (finding the right match, by chance)  females that mated with multiple males had a better chance of randomly sampling a male whose alleles happened to be a good match for her alleles - his dominant alleles masked her recessive alleles - made healthier babies together Tregenza & Wedell 1998, Evolution 52: 1726-1730 Rodríguez-Muñoz et al. 2010, Science 328:1269-1272

16. Benefits of polyandry II: Escape inbreeding Polyandry also allows females to escape costs of inbreeding - more mates = greater chance of at least one non-relative more eggs hatched when females mated with one sibling and one non-sib, compared to two sibs the non-sib’s sperm allowed her to produce higher quality offspring that completed development Tregenza & Wedell 2002, Nature 415: 71-73

17. Does polyandry benefit hermaphrodites? In A. willowi, all slugs are both male and female...  theory predicts that clutches with multiplesires should develop better, due to their greater genetic variability If a slug can tell he-she’s had more than one mate, he-she should produce more eggs or bigger eggs (sink more energy into offspring who are more likely to be healthy)

18. Does polyandry benefit hermaphrodites? swinger-slug experiment: (A)monogamy treatment - pairs of slugs held together for 3 weeks - eggs counted for last 4 days - also counted % of eggs that actually hatched “Oh great, you again.” “Stop poking me.”

19. Does polyandry benefit hermaphrodites? swinger-slug experiment: (B)polyandry treatment - sets of four “swingerslugs” divided into 2 pairs - swapped partners every 2 days (so each slug had 3 mates) - counted eggs + hatching as before, after 3 weeks of partner-swapping A C D B after 2 days.. A C D B swap

20. Benefits of polyandry Swingers laid more eggs than monogamous slugs - chose to invest more energy in reproduction when they had multiple mates Monogamous slugs suffered a higher % of defectiveembryos, usually a sign of a genetic mis-match

21. Why Cheat? Benefits of polyandry (female promiscuity) has been shown in turtles, birds, mammals, fish, insects, spiders... Overall, females may be under three forms of sexual selection: 1) choosing the fittest male (best alleles for offspring) 2) avoiding overstimulation by male display traits that exploit intrinsic receiver bias (but don’t reflect his fitness) 3) mating with enough males to give decent odds of getting sperm from at least one male that is a good match for her particular allele combination - hedge against an unlucky match, because females can’t know what recessive alleles they carry

22. Degeneration of the Y chromosome: return of the ratchet To keep male-advantage alleles out of the female genome, the X chromosome does not recombine with the Y - the Y is thus a clone, transmitted w/out change from father to son The Y chromosome eventually begins to degenerate due to accumulating mutations, due to the exact same causes discussed earlier for asexual reproduction: (1) Muller’s ratchet: bad mutations pile up over time (2) Background trapping of beneficial mutations Eventually, the Y ends up with few functional genes

23. Evidence the Y loses functional genes by background trapping (1) in D. miranda, part of an autosome translocated onto the Y - accumulated many bad mutations in genes on the new Y, compared to its autosome homologue (2) steroid sulfate gene is functional on mouse Y, but is not functional in humans (3) shown experimentally w/ flies (Rice, 1994) - make an autosome act like a Y (sex determining) by not letting it pass through females (throw out daughters) - after 35 generations, males had 47% lower fitness - evidence that non-recombining sex chromosomes quickly accumulate deleterious mutations

24. Evidence the Y loses functional genes by background trapping (4) in our fancy-tailed friend the guppy, sexy males have sexy sons -- but the sexier the son, the more likely he is to die... …when young, before developing his colorful ornaments …also when older fitness benefits of male-advantage alleles are balanced by: - fitness costs of ornaments... - or, hitch-hiking deleterious mutations that can only survive on super-sexy Y chromosomes Only benefit to females that chose sexy males is, they have sexy (but unhealthy) sons (and lousy daughters) Brooks (2000) Nature 406: 67-70

25. Full circle: gain and loss of the Y Trick females into mating more Collects a bunch of male-advantage alleles Y comes into existence (sex determined by one gene) Harm females by mating Lack of recombination with the X chromosome

26. Full circle: gain and loss of the Y Collects a bunch of male-advantage alleles Y comes into existence (sex determined by one gene) Mutations near the male-advantage alleles hitchhike onto Y Lack of recombination with the X chromosome Y keeps accumulating deleterious mutations

27. Full circle: gain and loss of the Y Collects a bunch of male-advantage alleles Y comes into existence (sex determined by one gene) Mutations near the male-advantage alleles hitchhike onto Y Lack of recombination with the X chromosome Y keeps accumulating deleterious mutations Degeneration of the Y X O sex determination (found in many insects)

28. In summary: think about sexual conflict in terms of… (1)Male-advantage alleles (i.e., bright color) - are good when expressed in males: attract mates - are bad when expressed in females: attract predators resolution: confinement to Y chromosome (females are safe) result: eventual deterioration of the Y (Muller’s ratchet) (2)Sexually antagonistic alleles (i.e., toxic seminal fluid) - help male assert his reproductive agenda over that of the females he mates with, to their harm resolution: females constantly counter-adapt (open-ended) result: arms race; each sex limits other’s adaptive evolution