Ethology Behavioural Ecology The Evolution of Mating Systems

Ethology & Behavioural Ecology The Evolution of Mating Systems Chapter 11 Alcock (Animal Behavior) Tom Wenseleers

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

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 Genetic monogamy EPC nesting with one partner offspring from one partner 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?

1. Monogamy

Monogamy 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.

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.

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

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

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

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.

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?

Costs vs. benefits of male sacrifice In most animals there 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.

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 females for 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.

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/X 1 > 1/N + 1/X • This is more likely to be true if N is large females mate with many males X is large male biased sex ratio • It can never be true if N is one females only ever mate to one male X is one or less males not more numerous than females • Translate back to biology Male sacrifice is more likely when females mate with many males and when the sex ratio is highly male biased. This confirms our intuition.

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.

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.

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

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.

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.

Burying beetle

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.

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.

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.

Mate guarding: rock-haunting possum Mate-guarding is facilitated by the small, discrete home ranges occupied by females of the rock-haunting possum.

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.

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

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.

Monogamy in birds Common Loon (ijsduiker). DNA study of 58 young from 47 families. All were offspring of the birds that 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.

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.

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.

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.

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.

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

In Tree Swallows polygynous males father fewer surviving young (0. 8 fledglings) than monogamous males (3. 0 fledglings).

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.

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

2 a. Polyandry

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 a wide range of hypotheses for "multiple mating" by females, all based on the idea that the female benefits from mating with multiple males.

Extra-pair copulations (EPC’s) in birds Even though monogamous males assist one primary female, males also seek EPC’s. DNA fingerprinting and microsatellite analysis has shown EPC’s to be very common, occuring in 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?

Why Female Polyandry or EPCs?

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

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

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

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.

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).

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.

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.

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

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.

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.

2 b. Polygyny

Polygyny: One male mates with two or more females Examples : Birds: Lark Bunting (dikbekgors), Red-winged Blackbird (epauletspreeuw) Dunnock (heggemus) Marsh Wren (moeraswinterkoning) Marsh Wren

Mammals: Lions, Gorillas, Bats. Also found in many fish, insects, etc.

Four basic types of polygyny 1. Female defense Polygyny 2. Resource defense Polygyny 3. Scramble competition Polygyny 4. Lek Polygyny

Polygyny Female defence polygyny Females in breeding condition aggregate. Males may then be able to monopolise a group of females. For example, male red deer or elephant seals. Males often fight with each other to control the females. Resource defence polygyny Females in breeding condition need access to some scarce resource. Males may be able to monopolize this resource. Females must allow the male to mate with them to have access to the resource. For example, wool carder bees. Males often fight with each other to control the resource.

1. Female defense Polygyny Common when females cluster in groups that are defensible. Males then become polygynous by defending such clusters against other males.

E. g. Elephant seals, lion prides, elk and deer herds.

In some marine siphonoecetine amphipods, which build protective cases out of gravel and shells, males collect females and glue their houses to their own.

Female defense polygyny in the greater spear-nosed bat Large male (bottom) guards a roosting cluster of smaller females.

In general, female defense polygyny possible because females cluster for their own reasons and males exploit this. E. g. Lionesses cluster to defend feeding territories. Deer gather for protection. Elephant seals gather on the few suitable nursery beaches.

Polygyny may be costly for females Number of offspring per female decreases with the number of females in the male harem. Females still remain part of the harem simply because driving off all other females might be costly.

2. Resource defense polygyny Male becomes polygynous by defending a resource that females need to produce young (food, nesting sites).

Resource defense polygyny in an African cichlid fish Lamprologus callipterus exhibits extreme sexual dimorphism (males 13 X times larger than females). Females lay eggs inside empty snail shells and remain inside shell until eggs hatch.

Resource defense polygyny in an African cichlid Males gather shells into large collections and defend them from rival males. The more shells the male can collect the more nesting sites it provides for females. Up to 86 shells have been recorded in one collection and up to 14 females at once. Extremely large male body size has been selected for because it enables males to collect shells and to defend their territories.

Resource defense polygyny in the black winged damselfly Male black-winged damselflies defend territories containing floating aquatic vegetation that females prefer to lay eggs on.

Resource defense polygyny in the carder bee (Anthidium manicatum) female Females collect plant hairs to use in nest building, hence the name wool carder bee. The males defend patches of flowers and aggressively drive off or even kill other bees. The female has to mate with the male to be allowed to forage on his patch of flowers. This is termed resource defence polygyny. male (grote wolbij) The male gets to have more than one female as he controls a resource that is valuable to the females.

Polygyny threshold model Some females choose to mate with already mated males who will not help them feed their chicks even though unmated males with territories are available. Why would a female do this? Polygyny threshold model: predicts that female will accept role of 2 nd mate (polygyny) when superior resources on males territory mean that female would do better there than as 1 st mate on a poor territory.

Curves represent payoffs to female. Female can choose between males A and B. A has a mate, B is unmated. Polygyny threshold model

Resource defense polygyny in red-winged blackbird Male Red-winged Blackbirds hold territory on marshes. Males with the best territories attract harems of up to 15 females. Females choose males on the basis of territory quality. Male’s red epaulettes are essential in male-male competition.

Polygyny threshold model: Lark Bunting Male Lark Buntings (dikbekgors) establish territories in grassy, open habitats. Mate with > 1 female but assist only first female to settle on their territory. Some female LB’s accept secondary female role on good territory to obtain a high quality nesting site. In bad nest sites young die from exposure to the sun.

Polygyny threshold model: pied flycatcher Some male Pied Flycatchers establish two territories. Sing to attract a female. Males provide little help to female on 2 nd territory, so female has low reproductive success.

Polygyny threshold model: pied flycatcher Each female mated to a polygynous male has lower reproductive success than a monogamous female. However, males' r. s. is higher than that of a monogamous male. Male Pied Flycatchers clearly try to deceive females into polygyny. Not clear yet if females really fooled or have no better alternative.

3. Scamble competition Polygyny When receptive females are widely dispersed males are best off not be territorial, but just to try the hardest to find a female. May result in one male mating with several females. E. g. Photinus fireflies. Other type of scramble competition polygyny: explosive breeding assemblage, when breeding season is highly compressed. Mad scramble for position to fertilize eggs. E. g. frogs, horseshoe crab. Usually associated with external fertilisation.

4. Lek Polygyny In lekking species males display for females at a predictable location (a lek) and females come to the site to choose mates. Males provide no resources except sperm, they do not help in raising the young. Examples: Grouse (korhoen) Ruffs (kemphaan) manakins Cock-of-the-rock (rotshaan)

Males display for females. Females choose males on basis of appearance and displays (sexual selection). Sage Grouse (waaierhoen) displaying on a lek

Highly skewed mating success is normal in lekking systems. A few males obtain most of the matings. By mating with best possible male, females obtain the best available genes for their offspring.

In well-studied Black Grouse (korhoen) and Sage Grouse (waaierhoen) lekking systems <10% of males obtain 70 -80% of the copulations.

Why do males gather in leks? Gathering in leks may reduce predation risk. Open country birds display in groups whereas forest species usually display solitarily. Birds-of-paradise that display in leks are edge or second-growth species (where predation risk is high) whereas primary forest species display solitarily.

Three most favored hypotheses for evolution of lekking are: 1. “Hot-spots” hypothesis 2. “Hot-shots” hypothesis 3. Female preference hypothesis.

1. Hot-spots Hypothesis: males gather at sites where they are likely to encounter females.

1. Hotspots hypothesis Lekking bees, wasps and other insects often use same locations for leks. Territories of lekking flycatchers, manakins and hummingbirds also often overlap. Gather along streams or ridgelines that act as highways for female movement.

2. Hot-shots Hypothesis: subordinate males cluster around most attractive males ― “hot-shots” ― in order to be seen by or to intercept females attracted to these males.

2. Hotshot hypothesis: great snipe In Great Snipe (poelsnip) removing central dominant bird caused neighbors to leave territories. Removal of subordinates resulted in their territories being refilled.

3. Female Preference Hypothesis: females prefer to choose from groups of males because comparisons are easier to make.

The mating behavior of the Ruff (kemphaan) appears consistent with all three hypotheses. Male ruffs are named for their well-developed ruffs, which they use to display to females (reeves).

Ruffs are polymorphic with ruffs occurring in a variety of colors.

Male ruffs use a variety of mating strategies. They pursue females (followers), wait for them at rich feeding ground (interceptors) or wait at classic leks (lekkers).

White-ruffed males appear to have evolved as specialist Followers skilled at tracking the movements of females between neighboring leks.

Male ruffs may switch tactics but committed lekkers have the highest mating success.

Dark morph ruff displaying to a female.

Controlled experiments suggest that female ruffs prefer larger leks. This preference increases the mating success of males at large leks and favors that breeding strategy.

Female ruffs prefer groups of at least five males and visit such groups more often.

Leks with >5 males do not attract more females, thus satellite males reduce success of dominant males by intercepting some of the females.

Hot-spots and hot-shots hypotheses also relevant to ruff mating system. Leks tend to be located by ponds where females come to feed (Hot-spots). Satellite males gather around most successful males (Hot-shots).

The clustering of males on leks may in part be due to a tendency of young or inexperienced males to gather near older or successful males. Such satellite males may get occasional matings and perhaps gradually improve their status. Such associations are most extremely developed in the Central and South American manakins.

Cooperative leks displays. In many manakins males perform cooperative displays. Three or four males may cooperate to display but usually only the alpha male gets to mate. Round-tailed Manakin

In Long-tailed Mankin males may take 8 years to move up to alpha position. Four year study: in 117 observed copulations only 8 of 85 males copulated. 90% of copulations by 4 males and 67% by one alpha male.

Manakin mating system works because birds are long-lived and females tend to return to where they mated before. As a result, the beta and lower-ranking males can expect to inherit a high-quality display ground and can afford to delay mating.