Sperm Competition and Cryptic Female Choice

1. Females often copulate with more than one male even though they don’t have same relationship between number of mates and reproductive success as males do.

2. This means that sexual selection can occur between sperm. a. Sperm from rival males can compete (~male-male competition). b. Females may choose sperm (~ female choice).

Why do females mate with many males?

1. Cost of Resistance a. Female gains no benefit by mating multiply except to avoid harm b. Female dung flies can drown as males struggle for possession

2. Material (or direct) benefits a. Mating with multiple males allows access to more resources b. Example: Females can gain access to resources on territory of male (dragonflies and damselflies). c. Example: May increase the amount of care provided by multiple males to offspring (dunnocks, Galapagos hawks)

2. Indirect benefits a. Fertility insurance: Reduce risk of having infertile partner. Test=look at fertilization success. b. Example: Polyandrous female Gunnison’s prairie dogs are pregnant 100% of the time while monogamous females are pregnant 92%.

3. Avoiding male harassment/infanticide a. Males that have a sufficient chance of paternity won’t commit infanticide.

Why do females mate with many males?

1. Songbirds provide some of the best evidence for females mating multiply to gain genetic benefits. a. Social monogamy doesn’t not mean genetic monogamy because female extra pair paternity is common. 10-40% of young may be sired by male not the female’s social mate depending on the species.

2. Females paired to attractive males tend to be more faithful. Females paired to unattractive males (as measured by the trait in table 7.3) actively seek extra-pair matings. Attractive males tend to survive better suggesting that they have good genes.

3. Test: Compare the success of extra-pair sired young with their within-pair sired half-siblings raised in the same nest. a. There is increased survival of extra-pair sired young in two different bird species: blue tits and collared flycatchers. Thus, females gain a genetic benefit from extra-pair matings

Species Attractive Trait of extra-pair Reference Table 7.3 In some male trait male compared to song birds, females social mate seek extra-pair matings from males Great reed warbler Song repertoire Larger Hasselquist et al. whose display traits Acrocephalus (1996) are more elaborate arundinaceus than those of their social mates Barn swallow Tail length Larger Saino et al. (1997) Hirundo rustica

Blue tit Cyanistes Ultraviolet Brighter Hunt et al. (1999) (Parus) caeruleus re!ectance of Kempenaers et al. crown feathers (1997)

Collared !ycatcher White patch on Larger Michl et al. (2002) Ficedula albicollis forehead Sheldon et al. (1997)

Consequences of Extra-Pair Mating

1. Extra-pair mating seems to be an important part of sexual selection. Can it explain the evolution of sexually dimorphic traits?

2. Owens and Hartley (1998) compared plumage dimorphism in species with information on rates of extra-pair paternity a. No correlation between degree of plumage dimorphism and number of social mates, but strong correlation between plumage dimorphism and rate of extra-pair paternity. b. Mating opportunities afforded by extra pair matings may help drive diversification in plumage coloration. Extra-Pair Mating

1. Why don’t females always pair with their most attractive male? a. When competition for the best mates is intense, females may be forced to settle for an unattractive mate. b. Good genes is just one part of the equation. Having a mate to provide parental care is important. But females may try to optimize both.

2. Constraints on extra-pair matings a. Social mate may reduce level of parental care in response to partner’s extra pair mating. i. In experiment where a female collared flycatcher was removed for an hour during her fertile period, her social mate reduced his effort in chick feeding. b. Attractive males sire higher quality sons but poorer quality daughters compared to less attractive males. i. Based on idea of sexually antagonistic genes, where an allele has high fitness in one sex, but low fitness in another. ii. Thus different sires may be best for sons vs. daughters. iii. Sexually antagonistic genes have been found in D. melanogaster and in red deer (Cervus elaphus).

Sexual conflict

1. Sexual conflict can occur whenever the optimal outcome of reproductive event is different for males and females.

2. Can lead to each sex evolving adaptations to favor the outcome towards its own interests a. Sexually antagonistic coevolution of traits in males and females

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Sexual conflict-over mating

1. For a given encounter it will usually pay a male to mate but a female to resist (due to the relationship between # of mates and reproductive success).

2. Male water striders will jump on a female’s back, grasp her, and attempt for force copulation. Females are more susceptible to predation and have reduced foraging abilities with a male on her back so already mated females try to avoid males. a. Correlated evolution in male morphology to increase grasping (elongation of grasping genitalia) and female morphology to resist (elongation of abdominal spines). b. Example of adaptations in one sex matched by counter adaptations in the other.

3. The conflict can also go the other way. a. Female songbirds try to gain extra-pair matings; social partner will follow her to try to prevent her from mating with other males.

Sexual conflict after mating: male adaptations

Male intra-sexual selection continues post-copulation in the form of sperm competition. The following are some adaptations by males for this competition.

1. Sperm removal: Female insects store sperm in spermatheca; males will either remove sperm from a previous male or pack it into the corners to ensure their sperm is used to fertilize the eggs.

2. Copulatory plugs: Male parasitic worms (Moniliformes dubius) will seal up the reproductive tract of females to prevent them from remating.

3. Altering mating ability of other males a. Male parasitic worms sometimes also seal up the reproductive tract of other males to prevent them from mating. b. Hemipteran insect, Xylocoris maculipennis, mates by males injecting sperm into the body cavity of females. A male can inject his sperm into a rival male. The sperm swim inside the body to the victim’s testes where they will be passed onto a female the next time the victim mates. Sexual conflict after mating: male adaptations

4. Anti-aphrodisiacs: Male Heliconius butterflies deposit a substance on the female after mating that discourages other males from mating with her.

5. Sterile sperm: ‘Parasperm’ are sterile, but are used to delay the remating time of a female by filling up her reproductive tract.

6. Accessory gland proteins (Acps): Male ejaculate contains proteins that influence female behavior and physiology. a. Drosophila melanogaster has at least 80 Acps. b. They increase female’s egg laying rate, decreasing her likelihood of remating, incapacitate rival sperm, etc. b. Increase male’s reproductive success, but decrease female’s lifespan.

Sexual conflict after mating: male adaptations

7. Strategic sperm allocation: Even though sperm is cheap to produce males don’t have a limitless ability to copulate. a. Adders loose as much body mass during spermatogenesis as when searching and competing for females.

8. Pizzari et al 2002 tested for strategic sperm allocation in feral fowl (Gallus gallus, ie chickens). Females were fitted with a harness that collected sperm that could be counted. a. Males increased sperm investment when there were more male competitors. b. Male allocated more sperm to females with larger combs, which lay larger eggs. c. A male’s sperm allocation decreased with repeated exposure to the same female, but renewed with the arrival of a novel female. This has been termed the “Coolidge effect.”

Sexual conflict after mating: female adaptations

1. Females can preferentially choose sperm from specific males to use to fertilize their eggs. This is known as cryptic female choice.

2. When female feral fowls are forced to mate with subordinate males they will eject his sperm immediately after copulation.

3. Experiments by Tregenze et al. on field crickets. a. When female field crickets are mated to two siblings they have a greatly reduced number of eggs that hatch (cost of inbreeding). b. When mated to one sibling and one non-sibling have equal hatching success as females mated to two non-siblings. c. Able to sort the sperm and use only from non-sibling male.

Sexual conflict: who wins?

1. Sexually antagonistic adaptations are likely to lead to ‘Red Queen’ dynamics where neither sex gains a long-term advantage.

2. Antagonistic coevolution demonstrated in Drosophila melanogaster a. Two selection lines created: 3 males and 1 female per vial (intense sexual selection) or 1 male and 1 female per vial (no intra-sexual selection). b. In monogamous line males decreased their courtship and mating rate and female survival and fecundity was greater than in the intense sexual selection line. c. Males evolved to be less harmful to females when guaranteed paternity. d. Females from monogamous line had significantly lower survival and reproductive success when mated to males from intense sexual selection line. e. Thus, monogamous females evolved to be less resistant to harmful male traits compared to females in intense sexual selection line. Sexual conflict: who wins?

1. Post-mating conflicts can also result in coevolution of genital morphology

2. Different species of male waterfowl have phalluses that vary in length from 1.5 cm to 40 cm. Length is correlated with the frequency of extra-pair matings.

3. Females have evolved extra spiral or pouches within their vaginas in response to elongated and elaborate phalluses.

4. Spirals are in the opposite direction to male phallus spirals suggesting antagonistic rather than mutualistic coevolution

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Chase-away sexual selection

1. Discovery of antagonistic coevolution between sexes led to new model of sexual selection: ‘chase-away sexual selection.’ Proposed by Holland and Rice (1998).

2. Chase-away sexual selection: males are selected to induce females to male and females then evolve resistance to male tactics/traits.

3. Drosophila selection experiments and waterfowl are examples of chase-away, but the hypothesis can also explain the exaggeration of traits males use to attract females.

4. Swordtails are an example of sensory bias, and also an example of chase-away selection. a. Female platyfish (males don’t have swordtail) have stronger preference for males with swordtail than female swordtail fish do. b. Female attraction for swords has declined as swords have evolved as predicted by chase-away.

Chase-away sexual selection

1. Chase-away sexual selection can also lead to polymorphisms

2. Ischnura elegans damselflies have one male type, but three color morphs for females: red, yellow and blue. Blue is actually a male-mimic.

3. Male mating harassment has favored female counter-adaptions.

4. Males form a search image for common females. Frequency-dependent selection causes rare females to have an advantage because they face less harassment .

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Summary of Sexual Selection by Female Choice Who Benefits from Sexual Selection? Good Genes Runaway Chaseaway Females + 0/+ - Males - 0/+ + Good Genes: 1. Females get indirect benefits = good genes for offspring survival. 2. Males maintain costly sexual signals and many males may not mate.

Runaway: 1. Considered non-adaptive with respect to naturally selected traits. 2. Females may get “sexy sons.” 3. Males with the trait have high reproductive fitness, but there may be naturally selected costs. Chaseaway: 1. Female reproductive fitness lowered. 2. Male reproductive fitness increased. 3. Continual arms race. Summary for Sexual Selection and Sexual Conflict

1. Asymmetries in investment leads to different selection pressures in males and females.

2. Sex that invests less is more competitive while sex that invests more is choosier.

3. Strong competition for mates (sexual selection) typically results in intense male-male competition (intra-sexual selection) and females being selective about which males they mate with (inter-sexual selection).

4. Females may prefer males due to either direct benefits, runaway sexual selection, sensory biases, or good genes benefits.

5. When males contribute to parental investment males may be choosy and females may compete for mates.

6. Sexual selection can continue after mating, in the form of sperm competition or cryptic female choice.

7. Sexual conflict and chaseaway sexual selection can occur when one sex tries to increase its fitness at the expense of its partner.

Sexual Conflict and Hermaphrodites

1. Simultaneous hermaphrodite animals: have both male and female sex organs.

2. Can be both a father and a mother at the same time.

3. Used to think that sexual selection (i.e. females choosing males) did not apply.

4. However, if sperm are cheap and eggs limiting, selection favors individuals that enhance the success of their own sperm, and selects against foreign sperm.

5. Can get greater reproductive success with “male” function, than “female” function.

6. Sexual conflict: the reproductive interests of the mating pair differ. Each is trying to maximize it own reproductive success.

Partner Manipulation in Banana Slugs

Partner Manipulation in Banana Slugs

Partner manipulation: Manipulate your mating partner’s phenotype to maximize your fitness, which often decreases your partner’s fitness. Love Darts in Snails and Slugs

1. During copulation, partners place large spermatophores in the spermatophore-receiving (SRO) organ of their partner.

2. The spermatophore is then digested in the SRO. Only ~0.1% of the spermatozoa escapes to where fertilization occurs.

3. Individuals shoot each other with love darts. The love dart is laced with hormones and increases the number of escaping spermatozoa from the SRO

4. By darting its partner, a snail can increase its chances of paternity.

5. The Japanese Euhadra subnimbosa uses its darts to stab its partner >3000 times during 22 min of ‘foreplay’ before copulation.

Diversity in Love Darts

Lesson: Sexual conflict can lead to diversification.

Love Darts in Snails and Slugs

1. Darts have evolved multiple times, and have been lost multiple times.

2. Darting species may be locked in sexually antagonistic selection which leads to an arms race of defense/offense.

a. SRO complexity correlates positively with dart shape (e.g. the presence of flanges).

Hermaphroditic flatworm, Pseudobiceros bedfordi. Have two penises, which they fence with. Each tries to smear the other with sperm, but tries to avoid getting smeared. Hermaphroditic flatworm, Pseudobiceros bedfordi.

St = areas with sperm

Hermaphroditic flatworm, Pseudobiceros bedfordi.

H = holes caused by sperm, Sc = Scars

Hermaphroditic flatworm, Pseudobiceros bedfordi.

* = Large hole where large amount of sperm hit Body then tore in two!

Lessons

1. Sexual conflict can be costly. Can impose a large selective force. Can lead to partner manipulation.

2. Even hermaphrodites have different interests when mating. Each is trying to maximize its individual fitness.

3. Sexual antagonism can select for diversity in weapons and mating behaviors. Mediating the Conflict

1. Many hermaphrodites inseminate reciprocally. This “sperm trading” ensures reciprocity during mating.

2. Test: Create cheaters by vasectomizing one partner of hermaphroditic sea slugs (Study by Anthes, 2005)

3. Result: Partners of the cheaters were less likely to trade intromissions/inseminations, and were more likely to terminate a mating encounter.

Further Reading on Wacky Mating Systems: Dr. Tatiana’s Sex Advice to all Creation