The Evolution of Mating Systems Chapter 11 Alcock (Animal Behavior) Tom Wenseleers

1. The Evolution of Mating SystemsChapter 11 Alcock (Animal Behavior)Tom Wenseleers Ethology & Behavioural Ecology

2. Aims & Objectives • Aims • Present the concept of alternative "mating systems" • Present a simple mathematical model for male monogyny • Present examples of different mating systems and factors that favour these particular mating systems • Objectives • Learn examples • Understand the underlying logic in the model of male monogyny • Understand why different conditions can favour different mating systems

3. Mating Systems There are many different mating systems including Monogamy one partner Polygamy more than one partner Polygyny one male, multiple females Polyandry one female, multiple males Polygynandry multiple females, multiple males Social monogamy nesting with one partner Genetic monogamy offspring from one partner EPC extra-pair copulation What is the cause of these different mating systems? Why, for example, does the male honeybee have a maximum of one partner and one mating while a male wool carder bee may mate hundreds of times with many different partners?

4. 1. Monogamy

5. Prolonged, essentially exclusive bond maintained with one member of opposite sex. Generally a rare system. Rare in mammals (except for some rodents, primates and dogs). However, is commonest avian mating system. Monogamy

6. Puzzle: Male monogamy Evolutionary puzzle: Males generally provide little resources to young and have an abudance of sperm with which they could fertilize several females. Hence, males would be expected to benefit from seeking extra mates (see previous lecture) Why don’t they? Monogamy is an armed compromise rather than a happy collaboration.

7. Male monogamy Several hypotheses:1. Mate-guarding hypothesis 2. Mate-assistance hypothesis 3. Female-enforced monogamy

8. 1. Mate-guarding hypothesis (MGH) Monogamy may be best choice if female would mate again if male deserted her and if 2nd male would fertilize eggs.

9. 1. Mate-guarding hypothesis (MGH) Mate guarding should pay off when females: 1. Are scarce and hard to find. 2. Remain receptive after mating. Example: Clown shrimp Receptive females are scarce and widely distributed

10. Male suicide as mate-guarding Honeybee drones mate only once and die after mating. The drone's genitalia break off during mating to form a mating plug. This does not stop the queen from mating with additional males during her mating flight, but it does prevent sperm from leaking out.

11. Male suicide as mate-guarding As we saw in previous lecture, the male redback spider may sacrifice his life during mating by placing his body directly into the female's jaws. Benefit: greater paternity from current mating. If the male was the first male to mate the female then the female is less likely to remate. If the male was the second male to mate the female then more of his sperm will fertilize her eggs. Cost: reduced or zero future matings. Cost vs. Benefit: when is male sacrifice favoured?

12. Costs vs. benefits of male sacrifice In most animals there are approximately equal numbers of sexually mature males and females. But in redback spiders and honey bees there are many more mature males. In redbacks this is because males mature when small. As a result, fewer males die before reaching maturity. In honeybees thousands of males are reared for each queen reared. The large male:female ratio favours male monogamy. It means that males will have lower mating success than females and that males are less likely to have multiple partners simply because females are rarer than males. This makes it more worthwile to increase the paternity success of the current mating even at a cost of fewer additional matings. The current mating is made more successful by plugging the queen to stop sperm leaking out or by prolonging the mating of the female spider to reduce her chances of remating.

13. Costs vs. benefits of male sacrifice • We can make a simple mathematical model to investigate when male sacrifice is worthwile. We will ask the question "Under what circumstances will a male who is mating with an unmated female have more offspring if he sacrifices his life to prevent her from mating again?" • We set up the following parameters X = the ratio of mature males to femalesfor an even sex-ratio X=1, for male bias X>1 Y = the number of offspring that a female has (cancels out) N = the number of mates per female, if not prevented by a male • The number of offspring of a sacrificing male who is mating with a previously unmated female = Y • The number of offspring of a non-sacrificing male who is mating with a previously unmated female = Y/N + Y/X. The Y/X is from future mating opportunities and the 1/X comes about because the male must compete with all the other males.

14. Costs vs. benefits of male sacrifice • The sacrificing male strategy is better if it results in more offspring. That is, if the following inequality is true:Y > Y/N + Y/X1 > 1/N + 1/X • This is more likely to be true ifN is large females mate with many malesX is large male biased sex ratio • It can never be true ifN is one females only ever mate to one maleX is one or less males not more numerous than females • Translate back to biologyMale sacrifice is more likely when females mate with many males and when the sex ratio is highly male biased. This confirms our intuition.

15. 2. Mate-assistance hypothesis (MAH) Male stays with partner because male assistance increases youngs’ survival. Increased survival of young outweighs extra young gained by seeking extra mate.

16. 2. Mate-assistance hypothesis (MAH) Example: Seahorse Hippocampus sp. Males carry eggs in a sealed brood pouch for over ca. 3 weeks. Male-female relationship is durable. They greet each other in the morning and ignore other seahorses of the opposite sex. Male can hold only one clutch, so no benefit in courting extra females. Females choose monogamy because males are scarce and because females are poor swimmers and thus vulnerable to predators.

17. 3. Female-enforced monogamy hypothesis (FEMH) In some species females actively prevent males obtaining extra mates.

18. Female-enforced monogamy The previous examples of spiders and honey bees considered only male interests. What if we also consider female interests? In the bee and spider examples, the female is not in conflict with the male. The honey bee queen is not prevented from mating with additional males by the presence of the mating plug, and neither is the female redback spider. Presumably, the female redback spider has a lower probability of mating again after cannibalizing a male during mating, because the longer duration of the copulation resulted in her being inseminated properly, thereby not needing to mate again.However, in some cases female interests may be involved and may result in a female preventing a male from mating multiple times. One example is from the burying beetle, Necrophorus. After setting up a nest with one female, the male may want to attract a second female. This may benefit the male as he will have two sets of offspring. However, it will be disadvantageous to the first female as her offspring will have to compete with the offspring of the second female for food. The logic is shown by the following made up numbers. Note that male and first female are in conflict over the male acquiring a second female. Male: one partner, 10 offspring; two partners, 6 + 6 = 12 offspring. Female: sole partner, 10 offspring: not sole partner 6 offspring.

19. Burying beetle: female-enforced monogamy Burying beetles, Necrophorus spp., are common in Belgium. The beetles are attracted to small mammal and bird corpses which they bury. The male and female and sometimes additional males and females build a nest containing the corpses and tend the larvae. A female burying beetle will attack her mate if he tries to release pheromones to attract other females to a carcass the pair have buried.

20. Burying beetle

21. Burying beetle: female-enforced monogamy After setting up the nest with the female, the male may try to attract a second female by emitting pheromone. This will be good for the male but not so good for the female as there will be increased competition for the food to rear the offspring. When the first female smells pheromone she pushes the male off his signalling perch. If the female is tethered she cannot do this and the male can signal more.

22. Razorbills: female enforced monogamy Males might benefit from additional partners but females may prevent them from doing so to monopolise their parental assistance. Razorbills nest in aggregations on cliffs. Females attack males that show an interest in a neighbouring female.

23. Monogamy in mammals • The mammalian traits of pregnancy and milk production by females make parental investment and care of offspring female biased. This should select for polygyny. Most mammals indeed are, but monogamy occurs in a few rare cases. • Monogamy in mammals may be connected with mate guarding. Social monogamy is correlated with situations in which females live apart in small territories, e.g. in possums. Mate assistance hypothesis may also apply to species with male parental care, e.g. prosimian primates, some rodents. • Polygynous males would have to leave a female while looking for other females. When they do this they leave themselves open to cuckoldry.

24. Mate guarding: rock-haunting possum Mate-guarding is facilitated by thesmall, discrete home ranges occupiedby females of the rock-haunting possum.

25. Mate assistance: Djungarian hamster Monogamous & male parental care Male helps infants being born. But: association between monogamy and male care not significant for all rodents or for primates overall.

26. Mate assistance: male care increases offspring numbers Male care of offspring affects fitness in the California mouse.

27. Mate assistance: offer protection against infanticide Other type of mate assistance: protect offspring against infanticidal male intruders. But: protection against infanticide hypothesis not supported by larger analysis.

28. Monogamy in birds Common Loon (ijsduiker). DNA study of 58 youngfrom 47 families. All were offspring of the birdsthat raised them. Similar in Florida Scub Jay(struikgaai) Most, 90%, of bird species have social monogamy. In some birds there is also genetic monogamy, but in ca. 70% of birds with social monogamy some of the female's offspring result from "extra-pair copulation" (EPCs) from non-partner males.

29. Comparing birds and mammals Why is social monogamy more common in birds than in mammals? Male assistance hypothesis: male birds, unlike male mammals, can feed young as well as females. A key prediction is that male parental care should increase the number of surviving young. This can be readily tested.

30. Male parental care in birds increases the number of surviving young (zwarte spreeuw) In the spotless starling, males whose testosterone levels were reduced by the anti-androgen cyproterone acetate (CA) provided more food for their broods and had the highest fledging rate per brood. Males given extra testosterone (T) provided less food and had the lowest fledging rate. Untreated controls were intermediate with respect to both feeding and fledging rates.

31. Male parental care in birds increases the number of surviving young Male assistance in Snow Buntings (sneeuwgors) is essential to rearing young. Females whose males were removed reared fewer than 3 young. Those with males reared 4 or more.

32. Male parental care in birds increases the number of surviving young In a population of starlings (spreeuwen) where some males helped their mates incubate their eggs and others did not, the clutches with biparental care stayed warmer. As a result, 97% of the eggs with biparental care hatched, vs. 75% for eggs with female uniparental care.

33. In many birds raising young is so hard, it takes a pair to rear even one young (e.g. albatrosses).

34. In Tree Swallows polygynous males father fewer surviving young (0.8 fledglings) than monogamous males (3.0 fledglings).

35. More offspring of polygynous males die because male can’t help both females (MAH). Females of polygynous males also mate with other males because male cannot guard two females effectively (MGH). Monogamy best for both male and female Tree Swallows.

36. 2. Polygamy Any mating system involving mating with and, in many cases, forming pair bonds with multiple members of the opposite sex. Two main kinds: Polyandry Polygyny

37. 2a. Polyandry

38. Puzzle: Female polyandry Another evolutionary puzzle is female polyandry. Expected that females cannot greatly increase the number of offspring by having multiple partners. However, by having multiple partners a female may be able to increase the number of offspring somewhat. For example, by mating with two males she is less likely not to be fertilized successfully. In addition, by mating with several males a female may benefit from additional paternal care to her young. By mating with several males, a female may also be able to increase the quality of her young. There are a wide range of hypotheses for "multiple mating" by females, all based on the idea that the female benefits from mating with multiple males.

39. Extra-pair copulations (EPC’s) in birds Even though monogamous males assist one primary female, males also seek EPC’s. DNA fingerprinting and microsatellite analysishas shown EPC’s to be very common, occuringin ca. 70% of all socially monogamous birds. Male benefits of EPC’s are obvious (increased offspring at low cost). But why would females seek EPC’s?

40. Why Female Polyandry or EPCs?

41. Fertility insurance: Gunnison' prairy dogs Monandrous females pregant 92% of the time. Polyandrous females pregnant 100% of the time.

42. Fertility insurance: EPCs in red-winged blackbird Female red-winged blackbirds (epauletspreeuw) who mate with multiple males have higher egg hatching rates.

43. Fertility insurance: yellow-toothed guinea pigs Female yellow-toothed guinea pigs who mate with multiple males have fewer stillborn young.

44. Good genes: Crickets Female crickets were given a choice of two males. They mated with one (S) and not the other (U). Male offspring of the S and U males were reared and themselves tested. Offspring of S males were more attractive to females. This shows that a female who is already mated may benefit from mating with a "sexy" male as her own male offspring will be more successful. The female will then have more grand-offspring.

45. Genetic compatibility: bluetroat Young of the bluetroat have a stronger immune response when they are the result of a within-pair copulation (WPY) than when they are the result of an extra-pair copulation (EPY).

46. Genetic compatibility: pseudoscorpions Polyandry boosts female reproductive success in a pseudoscorpion. Yet, no correlation is found between the number of offspring of different females produced from matings with the same male. So it's a matter of genetic compatibility.

47. More resources: blackbirds Red-winged blackbird (epauletspreeuw) females are allowed to forage on territories of males with whom they've engaged in EPCs. Truly monogamous females are chased away.

48. More resources: megachilid bees By mating with many males, females of this megachilid bee gain access to pollen and nectar in those males' territories.

49. More resources: butterflies In many insects (including hanging flies, crickets, butterflies) males transfer resources to the female during mating. Extra partners may mean extra nuptial gifts. This is supported by these data from Pierid butterflies where males transfer a nutritionally valuable spermatophore.

50. More resources: Dunnocks In Dunnocks, a female may have two partners. However, a male will only provide parental care if there is a chance that he is a father of the female's offspring. He does not determine this directly, but indirectly by whether or not he mated with the female. By allowing both males to mate with her, the female gets both to help feed the offspring. Females sollicit more matings from the partner that spends less time with them.