鄭先祐 (Ayo) 教授 國立台南大學 環境與生態學院 生態科學與技術學系 環境生態研究所 + 生態旅遊研究所 Chap.07 Mating Systems 鄭先祐 (Ayo) 教授 國立台南大學 環境與生態學院 生態科學與技術學系 環境生態研究所 + 生態旅遊研究所

Chap. 7 Mating systems Different mating systems Monogamous mating systems Polygamous mating systems Promiscuous mating systems The ecology and evolution of polygynous mating systems Multiple mating systems in a single population? Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

Monogamous mating systems Monogamy was rare in mammals, but it was much more common in smaller diurnal groups, particularly rodents. 範例：the oldfield mouse (Fig. 7.2) Excavated more than 500 oldfield mouse burrows, captured the individuals in each burrow, and then brought them into the laboratory. 90% of the offspring found in a family group were fathered by the male in their burrow (Fig.7.3) Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

Monogamy and fitness consequences Choosing a high-quality mate, a mate that would give their partners high relative reproductive success by siring attractive offspring, offspring with strong immune systems, and so on. Significantly more pups were born to pairs made up of a male and his preferred mate (Fig. 7.4A) Naïve male, a male who had no experience with either of the females. No difference (Fig. 7.4B) Ayo 2010 Ethology

Ayo 2010 Ethology

Proximate underpinnings of monogamy Prairie voles, dopamine, nucleus accubens (brain), linked affiliate (friendly) and aggressive behavior Activation of two dopamine-related receptors (labeled D1 and D2) was critical to the formation of long-term monogamous relationships. When D2 receptors were activated by dopamine, pair bonding was facilitated, whereas when D1 were activated by dopamine, pair bonding was inhibited. Ayo 2010 Ethology

Polygamous mating systems Polygyny – males mate with more than one female per breeding season Polyandry – females mate with more than one male per breeding season. Jacanas (水雉), a group of sex-role-reversed shorebirds, in which the males incubated the eggs and care for the young, and the females compete aggressively for multiple mates. Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

Female defense polygyny Australian wasp in genus Epsilon. Males mature earlier than females. Males are very territorial. Once a virgin female wasp emerges from her cell, the closest male present climbs on her back and mates with her. (Fig. 7.7) One male (left) on the nest and a female (at arrow) that is starting to emerge from a hole in the mud nest, and with whom he will mate. (Fig. 7.7) Ayo 2010 Ethology

Ayo 2010 Ethology

Three characteristics (female defense polygyny Females are short-lived and have low fecundity, receiving all the sperm they will ever use from a single male Females mate shortly after becoming adults, and Females are grouped close together in space. Ayo 2010 Ethology

Leks one well-studied form of polygyny is called lekking, or arena mating. Lekking, which has been studied in birds, mammals, amphibians, fish, and insects, occurs when males set up and defend small arenas called leks– temporary territories specifically for mating– that typically contain no apparent resources (no food or shelter, for example). Two questions: What benefits do females obtain from this form of polygyny? What benefits do males obtain? Ayo 2010 Ethology

The benefits that females may receive 兩個假說： Good genes with respect to health Sexy-son hypothesis 案例： sandflies Males defend small arenas that measure about 4cm in diameter. Females can choose freely among courting males, who emit a chemical attractant called a pheromone. Ayo 2010 Ethology

Good genes vs. sexy-son hypotheses Compared the survival of offspring that were the product of females that were forced to choose among a random sample of males (part 1) and the offspring of females that were forced to choose between less attractive males (part 2). No evidence for the good genes model was uncovered. Support the sexy-son hypothesis When male offspring from part 1 and part 2 were placed in a lek, females showed a stong mating preference for the former. Ayo 2010 Ethology

Peacock Peacock living in Whipsnade Park in England. These peacocks divide up into many different leks, and males defend their arenas within the leks all day during the breeding season. A molecular genetic analysis to determine whether individuals in a lek were genetic kin, they found that indeed they were, with the average genetic relatedness within the groups being equivalent to that of half-siblings. The peacocks were able to gauge genetic relatedness and clustered near genetic kin within their leks. Ayo 2010 Ethology

Four males gather on a lek before any females arrive to observe them When a female appears on the lek, the male displays his tail in an attempt to get her to choose him as her mate. Ayo 2010 Ethology

Phylogenetic history of polygyny in warblers Family of birds known as Acrocephaline warblers. Three known facts Mating system vary from monogamous to polygynous Warblers in monogamous systems show much higher levels of parental care than do warblers in polygynous systems, with monogamous males providing much more food to chicks than do polygynous males. Warbler species in ranging from poor habitats with little food, to much better habitats that contain significantly more and better food types. Ayo 2010 Ethology

The polygynous great reed warbler The monogamous Seychelle warbler Ayo 2010 Ethology

Phylogenetic history of polygyny in warblers A strong correlation between mating system and habitat quality Most monogamous systems were found in poor habitats, and most polygynous systems were found in better habitats. Phylogeny of warbler mating systems (Fig. 7.10) (A) paternal effort is represented as the proportion of a pie chart that is green. (B) the relationship between paternal care and food supply is shown by the data points. Ayo 2010 Ethology

Ayo 2010 Ethology

Where there was less food, there was greater paternal care; where there was more food, there was less paternal care. Ayo 2010 Ethology

Polyandry in social insects Polyandry has been well-studied in social insects, where a single queen will often mate with many worker males. Compared to cases of nests where a single male mates with a queen, polyandrous nests often have greater levels of within-group conflict (Fig. 7.11) Less within-colony harmony The presence of numerous “patrilines”, that is, offspring descended from different fathers. Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

Adopting a polyandrous mating strategy Sperm replenishment Female avoids the cost of storing sperm Material benefits Nutrients, reduced predation, protection from other males, access to superior feeding sites, male parental care. Genetic benefits Replacement of “inferior” sperm Convenience Female avoids the costs of fending off copulation attempts by male. Ayo 2010 Ethology

Promiscuous mating systems When polyandry and polygyny are occurring in the same population of animals, the breeding system is said to be promiscuous(混雜的). 案例：Barbary macaque (Macaca sylvanus) During their estrous period, female Barbary macaques search for new male mating partners after each copulation. Female will mate different males. Male having numerous female sexual partners. Ayo 2010 Ethology

Several males form pair bonds with several females simultaneously. polygynandry Several males form pair bonds with several females simultaneously. 案例： dunnock (Prunella modularis) One or two males were resident on a female’s territory. (Fig. 7.13) The more help a polygynandrous female received, the higher the mean nestling weight of the chicks in the brood and the lower the chick mortality rate due to starvation. Ayo 2010 Ethology

A female with a newly hatched offspring. A female feeding her brood. Ayo 2010 Ethology

Female territories are shown in green, while alpha male territories are depicted by solid red lines and beta male territories are shown by dashed red lines. We can find mating systems ranging from monogamy to polygamy, polyandry, and polygynandry. Ayo 2010 Ethology

Menstrual bleeding and promiscuity Menstruation is a defense that has evolved in females to rid the female reproductive tract of pathogens carried in by sperm. Menstruation should be most common in promiscuous breeding systems. Promiscuous breeding systems not only expose females to greater quantities of sperm, but to a greater diversity of sperm, and hence to a greater diversity of diseases that use sperm as vectors. (Fig. 7.14) Ayo 2010 Ethology

Ayo 2010 Ethology

The ecology and evolution of polygynous mating systems Polygyny and resources The polygyny threshold model (PTM) How the PTM works The PTM and mate choice in female birds The PTM and human female mate choice Extrapair copulations Sperm competition Ayo 2010 Ethology

Polygyny and resources A female can often fertilize all her available eggs by mating with one or a very few males. Females track resources Female fecundity is not so much tied to the availability of mates as it is to the availability of resources, for example, food, defense, and so forth. Males track females Males, on the other hand, can potentially fertilize large numbers of females, and so male reproductive success is more tightly associated with access to females than with access to resources. Ayo 2010 Ethology

Distribution of resources If resources are dispersed fairly homogeneously If resource are clumped, males may be able to mate with and defend several females at once. Females live together for easier access to resources and for protection from predators. Ayo 2010 Ethology

The polygyny threshold model (PTM) How the PTM works Imagine that ten males each have their own territory, and that these territories vary with respect to some resource that is valuable to females. Male 1’s territory representing the area with the most food and male 10’s territory that with the least food. The first female arriving to choose a male … The second female choosing.. (Fig. 7.15) 案例：lark buntings (Fig. 7.16) Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

The PTM and human female mate choice Kipsigi tribe of Kenya The number of wives was strongly affected by the size of his territory– with larger, and presumably more resource-rich, territories came an increase in the number of wives. Ayo 2010 Ethology

In the Kipsigi population, polygyny is the norm In the Kipsigi population, polygyny is the norm. Kipsigi “co-wives” both relax (A) and work (B) together. (C) a man with many wives will have numerous huts, grain stores, strips for maize, and so on. Ayo 2010 Ethology

Ayo 2010 Ethology

Extrapair copulations Males and females were leaving their territories during the mating season and mating with other individuals, usually those in nearby territories. (Extrapair copulations, EPCs) Social monogamy and genetic monogamy The increased reproductive success of males who leave territories and engage in EPCs is clear, as they can fertilize more females. But why would a female be involved in EPCs? Ayo 2010 Ethology

Females be involved in EPCs Increase the probability that all their eggs are fertilized Maximize genetic diversity in their offspring Use EPCs to select males who have good genes Increase the amount of direct benefits– food, protection, and so on– that they receive from male. Ayo 2010 Ethology

About 13% of all mating were EPCs. Indigo buntings About 13% of all mating were EPCs. Females generally resisted EPCs to a greater extent than mating with their nesting partner, with the females resisting EPCs in 34 out of 43 attempts, while only resisting mating with their pairmates in 72 out of 320 attempts. Using electrophoretic comparisons, 257 young that were biopsided, 37 had genotypes that were not consistent with the genotype of one of their presumed parents. (about 13% EPCs) Ayo 2010 Ethology

A female indigo bunting A male indigo bunting Ayo 2010 Ethology

(A) Extrapair copulations Ayo 2010 Ethology

(B) Within-pair copulations Ayo 2010 Ethology

Sperm competition In some promiscuous mating systems, males compete not only for access to mating opportunities with females, but directly for access to eggs. Sperm storage occurs in sperm storage tubules (SST) at the uterovaginal junction. (Fig. 7.20) Females can store sperm from multiple males, setting the stage for sperm competition. Only a small proportion of sperm makes it into the SST. Ayo 2010 Ethology

Ayo 2010 Ethology

Sperm competition in dungflies Dungflies use the droppings of large, often domestic, animals as their choice site for breeding. While in most insects, copulations often last a matter of seconds, in dungflies they can last on the order of thirty minutes or more. Ayo 2010 Ethology

Ayo 2010 Ethology

The last male precedence The number of eggs that were fertilized by the last male to mate with a female was proportional to how long such a mating lasted. The longer the last mating, the greater the reproductive success of the male. (Fig. 7.22) Ayo 2010 Ethology

Ayo 2010 Ethology

Sperm competition in sea urchins It can also play an important role in species that do not have internal fertilization. Sperm’s swimming speed and fertilization success. To fertilize the same number of eggs, males who produced slow-moving sperm needed to release up to 100 times more sperm than males who produced fast-moving sperm (Fig. 7.23) Ayo 2010 Ethology

Ayo 2010 Ethology

Sperm competition in sea urchins Sperm decrease their swimming speed with age. (Fig. 7.24) (A) in sea urchins, older sperm swim slower, (B) a greater quantity of such sperm is needed to achieve high fertilization rates. As they aged, they were much less likely to fertilize an egg, even when they encountered one. Ayo 2010 Ethology

Ayo 2010 Ethology

Ayo 2010 Ethology

Other effects of sperm competition Kamikaze sperm hypothesis Natural selection might favor the production of some sperm types that are designed to kill other males’ sperm rather than fertilize eggs. Variability in sperm morphology (Fig. 7.25) Ayo 2010 Ethology

Ayo 2010 Ethology

Sperm number in humans Sperm competition has effects o the number of sperm produced per ejaculate. Data on the interval between copulations in a given pair of individuals, and assumed that the longer this interval, the greater the chances that a partner would have been unfaithful. Obtained sperm samples from individuals the next time they copulated with their partner. the number of sperm ejaculated during a copulation is a function of the time since a pair last copulated. (Fig. 7.26) Ayo 2010 Ethology

Sperm number in humans When couples spent more time together, and hence the risk of extrapair copulations was low, sperm count was significantly lower than when couples spent less time together. Ayo 2010 Ethology

Ayo 2010 Ethology

Multiple mating systems in a single population? Dunnocks: the long-term persistence of monogamy, polygyny, polyandry, and polygynandry in the same population. Battle of the sexes Fitness of males: polygyny > monogamy > polyandry Fitness of females: polyandry, polygynandry > monogamy > polygyny Females appear to be winning this battle: 75% of females and 68% of males observed were involved in either polyandrous or polygynandrous mating groups. Ayo 2010 Ethology

The battle of the sexes: territory size Difference between monogamy and polygyny is a function of male territory size. Difference between polyandry and polygynandry was a function of female territory size. Ayo 2010 Ethology

Supplementing the food on dunnock territories led to a decrease in female territory size but not male territory size. Ayo 2010 Ethology

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