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The Evolution of Reproductive Behaviour Chapter 10 Alcock (Animal Behavior) Tom Wenseleers. Ethology & Behavioural Ecology. Plan of talk. Evolutionary origins of two sexes Typical sex roles Reversed sex roles Male-male competition Female choice. Aims & Objectives. Aims

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The Evolution of Reproductive Behaviour Chapter 10 Alcock (Animal Behavior) Tom Wenseleers


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    1. The Evolution of Reproductive BehaviourChapter 10 Alcock (Animal Behavior)Tom Wenseleers Ethology & Behavioural Ecology

    2. Plan of talk • Evolutionary origins of two sexes • Typical sex roles • Reversed sex roles • Male-male competition • Female choice

    3. Aims & Objectives • Aims • Present a simple model for the evolution of male (small gamete) and female (large gamete) roles. • How sex differences in parental investment select for typical sex roles (e.g. choosy females) + exceptions • Objectives • Learn examples • Understand the evolutionary logic in the evolution of gamete size differences and typical sex roles

    4. 1. Evolutionary origin of two sexes:small gametes (males) & large gametes (females) NOT IN TEXTBOOK!!

    5. Origin of gamete size differences Will the mutant producing smaller gametes be selected for? Model Maynard SmithAssume small gametes are half size and that the mutant can make twice as many as a result.Yes If survival of smaller embryo is >50% that of normal embryoNo If survival of smaller embryo is <50% that of normal embryoNote that small embryo is 75% the size of the large embryo, and that when rare (i.e. new mutant) small gametes only fuse with large gametes. We are only considering "invasion" conditions, meaning a rare small gamete mutant in a population making large gametes.

    6. Graphical model The curve represents the survival of the immature individual as a function of the size of the embryo resulting from the fusion of two gametes in an ancestral situation when gametes were of one size.

    7. Graphical model The tangent from the origin shows the size of the embryo,a, that maximises survival per unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is the values on the survival curve).

    8. Graphical model The tangent from the origin shows the size of the embryo,a, that maximises survival per unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is the values on the survival curve).

    9. Graphical model The optimal size of a gamete is half of the optimal size of an embryo.

    10. Graphical model Would making half sized gametes be favoured? Yes. A half size gamete fusing with a normal gamete results in an embryo 75% the normal size with survival b. And making twice as many half size gametes gives more surviving offspring since 2.b > a.

    11. Conclusion • The model in the previous slides presents the idea that from an initial situation of equal-sized gametes, it is possible for smaller gametes to be at an advantage. In other words for two sexes to evolve in a sexually reproducing population in which there is initially only one sex. • However, the advantage of the smaller gametes will decrease as they get more common if fusion is at random. E.g., if two small gametes would fuse the embryo might be too small to survive. We might expect small gametes to evolve the ability to avoid fusing with each other. This would cause the evolution of two distinct mating types, males and females.

    12. 2. The evolution of typical sex roles

    13. Typical sex roles Angus Bateman & Robert Trivers: typical male and female sex roles come about because of sex differences in investment in individual offspring. MALESinvest little in each offspringcan potentially have large numbers of offspringcan greatly increase fitness by having multiple partnersrarely can increase fitness by being choosy FEMALESinvest a lot (more than males) in each offspringcannot, potentially, have large numbers of offspringcannot greatly increase fitness by having multiple partnersusually can increase fitness by being choosy

    14. Angus John Bateman Robert Trivers

    15. Males: typically brightly coloured as a result of female choicemales are usually morebrightly coloured to attractfemales male female gang gang cockatoo

    16. Males: typically larger as a result of male-malecompetition males are usually larger andstronger than females male female orangutan

    17. Eager males and choosy females # fertilisable females < sexually active males (♂-biased operational sex-ratio) selects for “eager” males and “choosy” females males should frequently want to mate with females when they don’t want to females should be choosy and reject low-quality males

    18. Coercive sex Not enforced Long courtship Enforced No courtshipStruggle Iron cross blister beetle

    19. Traumatic insemination spermalege Male bedbugs have a saber-like penis that they insert directly into the abdomen of their mates prior to injecting them with sperm. Such traumatic insemination may have evolved to overcome female choosiness. Female counterdefence: spermalege (modified region of abdomen where male pierces female).

    20. A counteradaptation to male sexual exploitation simulated peniswith sterile needle simulated peniswith dirty needle

    21. Another female counterdefence Dunnocks (heggemus): females eject sperm of low-status males Davies Nature 1983

    22. Females: typically more choosy Clark & Hatfield J. Psych. Hum. Sex. 1989 Males Females “Would you go to bed with me tonight?” “Would you go out with me tonight?”

    23. Females: typically more choosy Clark & Hatfield J. Psych. Hum. Sex. 1989 Males Females “Would you go to bed with me tonight?” 75% 0% “Would you go out with me tonight?” 50% 56% But sex roles still much more equal in humans than in any other primate, because of the large contribution of males in the upbringing of children.

    24. Test: sex role reversal • How can we test Trivers' idea that typical sex roles come about because of sex differences in investment in individual offspring? For example, that females are more choosy than males because they invest more in the offspring, and so are limited in the number of offspring by how much they can invest. • We predict that there will be sex role reversal in those species where males invest a lot in offspring. For example, because the male provides a costly nuptial gift to the female, or provides costly parental care to young.

    25. Pipefish: males that get pregnant Hippocampus: brood in pouch Syngnathus: brood in pouch Phyllopteryx: brood on tail

    26. Sex role reversal in pipefish • Males get "pregnant" and provide oxygen and nutrients to a clutch of eggs held in an egg pouch • During the time of male pregnancy females of some species (e.g. Syngnathus scovelli) can produce enough eggs to fill 2 male pouches. • Given an even sex ratio, male pouch space is therefore in short supply. • Males in these species tend to be sex role reversed, and tend to be choosy (they select females which provide the most eggs) • However in other genera, e.g. Hippocampus, the female egg laying rate is limiting. In these there is no sex role reversal.

    27. Sex role reversal in pipefish

    28. Nutritious spermatophores In many insects, the male transfers nutrients with his sperm or provides a resource for the female to eat when mating ("nuptial gift"). This has been much studied in Orthoptera (crickets, grasshoppers).

    29. Sex role reversal in Katydids A female of the Australian Katydid Kawanaphila eats a spermatophore whilst sitting on a pollen-poor kangaroo paw flower.

    30. Sex role reversal in Katydids If the difficulty of making nuptial gifts changes, then this may change choosiness. Males should be more choosy when the resources needed to make the nuptial gift are scarce. This was tested in the Australian Katydid Kawanaphila. Food supply varies greatly through the breeding season. When food is limited to pollen-poor kangaroo paw flowers spermatophores are hard to produce, and so very valuable. The males are often choosy and the females compete for males. But when food is abundant males rarely are choosy and females do not compete for males.

    31. Sex role reversal in Katydids Male Katydids provide a large nuptial gift at mating. Males are choosy when the resources (pollen) needed to make the gift are scarce.

    32. Sex role reversal in mormon crickets Mormon crickets are large, flightless Orthoptera. Males transfer an enormous edible spermatophore to females when they mate as a nuptial gift. Constitutes 25% of a male's body mass.

    33. Sex role reversal in mormon crickets Males transfer an enormous edible spermatophore to females when they mate as a nuptial gift. This constitutes 25% of male's body mass. Males probably can mate only once. Females can produce several egg clutches, provided that they can persuade several males to mate with them. Males put more resources in, so the operational sex ratio is female biased. That is, there are more females looking for males than vice versa. High densities of mormon crickets can form. When this happens, males stridulate. Females come quickly to the male, and jostle to compete for chances to mate with him. Males exercise choice over which females to mate with, preferring larger females who will be more fecund. That is a male chooses a female who will be able to lay more eggs fertilised by his sperm.

    34. Sex role reversal in mormon crickets

    35. Sex role reversal in mormon crickets Being choosy is beneficial for males of the mormon cricket (USA). They mate with larger, more fecund, females.

    36. Sex role reversal:the wattled jacana Male uniparental care Causes male to carry most of the cost of offspring productionResults in choosy males and ornamental, eager females Most birds have biparental care, and these do not show sex role reversal Emlen et al. 1998

    37. Conflict over sex roles in hermaphrodites: flatworms both want to become the male(minimum investment)"penis fencing": first one who is stabbed by the other’s penis becomes the female and has to produce expensive eggs Pseudobiceros hancockanus Michiels, N.K., and L.J. Newman. 1998. Sex and violence in hermaphrodites. Nature 391(Feb. 12):647

    38. Conflict over sex roles in hermaphrodites: banana slug penis chewing: the one whose penis is bitten off first becomes the female can take 12 hours A.B. Harper 1988, B.L. Miller 2005 Banana slug

    39. Sexual selection • Charles Darwin: made a distinction between natural selection (acts on individual survival) and sexual selection (acts on likelihood to mate) • intrasexual selection: competition withinone sex for mating opportunities, e.g. male-male fights • intersexual selection: likelihood to mate affected by interactions between the two sexes, e.g. as a result of female choice

    40. Male ornaments Antlers selected due to female choice male-male competition intersexual competition intrasexual competition European stag beetle red deer quetzal red deer peacock

    41. 3. Male-male competition

    42. Male-male competition • Male-male competition manifests itself in a wide variety of adaptations on the part of males, many of which have a strong behavioural component. • Fighting and selection for large body sizeAlternative mating tactics alternatives that are equally rewarding alternatives not equally rewarding (best of a bad job) Mate guardingSperm competitionetc... etc...

    43. Fighting

    44. Developmental costs Males of the dung beetle fight for mates. Beetles with long horns (left) have a fighting advantage but tissue that goes into horn construction (blue) is unavailable for the building of eyes (yellow). As a result, males with long horns (left) have smaller eyes than rivals with short horns (right). Both types may well be equally fit.

    45. Body size and mating systems in seals In seals, there is strong correlation between sexual dimorphism and polygyny. The sexes are of similar size in species where males cannot monopolise a large number of females. Where males can monopolise a harem of females, there is an advantage to large male size and this results in greater size dimorphism.

    46. Body size and mating systems in seals Elephant seal males can weigh 2000 kg. They fight vigorously and dangerously. The winner (beachmaster) commands a harem of dozens of females. The other males skulk away and get few or no matings. But maybe in a future year one of them will be the beachmaster. We can show that fighting is to acquire mates by correlating male dominance with mating success.

    47. Body size and mating systems in seals McCann's work on southern elephant seals on South Georgia. Recent DNA analysis shows that mating success is tightly linked with paternity.

    48. Sexual dimorphism Big elephant seals can win fights with other males and thereby get high reproductive success by monopolizing a lot of females. There is therefore tremendous selection pressure on elephant seal males to get large. But it takes a lot of time and energy to get big. We can predict that costly investment in the growth and maintenance of large bodies will only occur when exceptional rewards are accrued by large individuals. Also, there will come a point where there is no longer any individual advantage of growing larger or being more fierce (recall the hawk-dove game). Where mating occurs is also very important. If males cannot access and monopolise many females then extreme dimorphism should not occur. E.g., if mating occurs in the ocean vs. on the beach.

    49. Dominance correlates with reproductive success In Savanna baboons in Kenya there was a strong correlation between male dominance rank and the ability to monopolize fertile females across all groups studies.