Ecological benefits of cooperation. Life Insurance. Life Insurance. Fortress defense
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1 Ecological benefits of cooperation 1. For cooperation and eusociality to evolve it also is required that ecological conditions lead to a high enough benefit/cost ratio to favor cooperation a. Need B/C >1 so more efficient to raise siblings than own offspring 2. Three ecological factors may have been important for evolution of eusociality a. Life insurance b. Fortress defense c. Food distribution Life Insurance 1. Females may die while raising offspring, in which case the offspring are likely to die. 2. Females that cooperate with others in brood care have an insurance policy if they die because other females would continue brood care. 3. Example: The social wasp Ropalidia marginata has a development period of 62 days from egg to adult. A reproductive female only has only a 12% probability of surviving for 62 days. a. Females are able to increase their reproductive success by 3.6-fold by nesting in a group. Life Insurance 1. Field et al (2000) experimentally removed helpers from nests of tropical hover wasp Liostenogaster flavolineata. 2. Removal of helpers reduced number of small larvae reared, but groups that had more helpers post-removal able to rear more offspring. 3. Females can increase number of offspring successfully raised by 2.4fold by helping rather than breeding independently 3 Fortress defense 1. Needing to protect a food source or nest territory may favor staying at natal nest and eusociality. a. Food can be plentiful locally, but migration risky. In this case juveniles may require little feeding care. The first workers can develop as soldiers for protection of the food source/nest. 2. Gall-forming aphids, Pemphigus spyrothecae, have soldier caste that defends colony against insect predators (ladybug larvae). Aphids reproduce clonally so siblings have a relatedness of 1; workers are still equally related to siblings and own offspring. Thus need B/C >1 to help. a. Foster (1990) manipulated composition within gall to contain either 10 soldiers or 10 non-soldiers and then introduced a predator. b. In colonies with soldiers, predators were usually killed with few soldiers being killed c. In colonies with non-soldiers, the predator survived and all the aphids were killed and eaten.
2 Ecological benefits of cooperation Social insects can be divided into two groups, depending on if the main ecological benefit of sociality is life insurance or fortress defense 5 Ecological benefits of cooperation 1. Sponge-dwelling shrimp (Synalphaeus spp.) live in and consume sponges 2. Within sponge individuals live in social groups that vary from heterosexual pairs, to groups with multiple breeders, to eusocial colonies with a single queen and hundreds of sterile workers 3. Greatest competition for resources is from conspecifics or closely related species. All species are territorial and have fightings claws used in communication and combat (sometimes called snapping shrimp because of sound they make with their claws). 4. Eusociality is predicted to enhance to ability to defends sponges. Indeed, eusocial species appear to outcompete less social species because they are more abundant, occupy more sponges, and have broader host ranges. Food distribution 1. Mole-rats are the only examples of eusociality in mammals. They are small African rodents that live underground and dig tunnels to search for roots and tubers. a. There are solitary species, group living species (max. group size ~15), and two eusocial species (naked and Damaraland, max group size = 300 and 40 respectively). 2. Evolution of cooperation and eusociality thought to be due to food distribution a. Solitary species live in areas with consistent rainfall and a more even distribution of food b. Eusocial species live in dry areas where rainfall is unpredictable. Low rainfall means soil is hard and energetically costlier to dig tunnels in. Food is more patchily distributed and foraging riskier. When food is found often enough to feed entire colony for extended period. 3. A comparative study of 12 species of mole-rats found larger groups associated with lower density of food and greater variation in rainfall. Conflict within insect societies 1. Kin selection can be used to predict not only when to expect cooperation but also when to predict conflict a. Conflict occurs when one individual tries to obtain a disproportionate share of reproductive success
3 Sociality in Hymenoptera 1.In some species of social Hymenopterans, workers still have functional ovaries. 2.These species allow us to understand the conditions and conflicts that occurred before eusociality. 3.Paper wasp Polistes dominulus. Many workers are full sisters and get indirect benefits from helping. a. A third of all helpers are not closely related. 10 of 13 observed takeovers were of resident helpers. Helpers may inherit the nest, which is another reason to work. 4.Concession theory: dominant females may concede more reproductive chances to unrelated helpers than to close relatives. a. Supported by work on Polistes fuscatus. Testing Concession Eusociality Theory From Reeve et al 2000 Dominant female s share of production of daughers Conflict within insect societies 1. Kin selection can be used to predict not only when to expect cooperation but also when to predict conflict a. Conflict occurs when one individual tries to obtain a disproportionate share of reproductive success 2. In hymenopterans there are two main areas of reproductive conflict when there are fixed worker castes: sex ratio and who should produce male eggs 3. When conflicts happen how are they decided and who wins (queen or workers)? 1. Queens are equally related to her sons and daughters (0.5) and so like diploid females of any sexual species she is expected to invest equally in the two sexes (Fisher s theory of equal investment) 2. This only refers to equal investment in reproductive offspring, not sterile workers 3. A 50:50 sex ratio is stable because the expected reproductive success of a male and female is the same 4. If the queen produces an equal sex ratio workers spend their lives rearing equal numbers of brothers (r=0.25) and sisters (r=0.75). Average relatedness to reproductive siblings therefore is only 0.5, exactly the same if workers produced their own offspring
4 1. In order for a female worker to gain the full genetic benefit from staying at home and rearing sisters they must rear more queens than drones 2. But if they rear too many sisters then the sex ratio in the population will become so female-biased that a drone will have a much greater reproductive success than a queen 3. Stable sex ratio from the worker s perspective is 3:1 in favor of reproductive females a. When female reproductives are 3x as common as males, drones have 3x the expected success of queens because each drone has 3x the chance of finding a mate. b. From the worker s perspective this compensates for the fact that brothers are only ⅓ as closely retailed as sisters are. c. Total gain per unit investment via brothers and sisters is the same 1. If queens prefer a 1:1 sex ratio and workers prefer a 3:1 in favor of females, who wins the conflict of interest over the sex ratio? 2. Trivers and Hare (1976) analyzed the ratio of investment in male and female offspring in 21 species of ants a. Species were chosen because colonies contained only one queen who mated only once. 1. Concluded that the workers win the conflict and successfully manipulate the sex ratio towards their own optimum. a. The observed ratio is close to a 3:1 investment favored by workers. 2. Workers may thus have a lot of control in the colony, which is different from the idea of workers as subordinate females making the best of a bad job. 3. More conclusive evidence for worker control of sex ratio has been found by comparing sex ratio variation between colonies within a single species. 1. Within a single species some colonies have been found to produce either all or a majority of males while other colonies produce mainly females 2. Split sex ratio predicted when workers control the sex ratio and relatedness between sisters and brothers varies across colonies (queen either mated once or with multiple males) a. If two sisters fathered by different males they would have the same relatedness that a sister and brother share 3. In colonies where queen mated once predict workers to favor 3:1 sex ratio that is biased towards queen production 4. In colonies where queen has mated multiply, a less biased sex ratio is predicted. But the best sex ratio to produce depends on the population sex ratio.
5 5. Female biased sex ratio in some colonies increases reproductive success and value of males. 6. This then selects for colonies with multiply mated queens to invest more in reproduction of males. a. Decreases the value of males at population level leading to colonies where the queen only mated once to produce females to an even greater extent. 7. Feedback results in colonies with singly mated queen producing either all or predominantly females and colonies with multiply mated queen producing all or predominantly males. a. Maximizes genetic contribution to next generation for both singly mated and multiply mated colonies 1. Sundström (1994) used allozyme markers to determine how many times queen wood ants (Formica truncorum) had mated 2. Compared sex ratio of reproductives in colonies founded by queen that had mated once with colonies where queen had mated multiply. 3. Found that colonies with singly mated queens produced predominantly females and colonies with multiply mated queen produced predominantly males. Mechanisms of sex ratio conflict 1. If workers manipulate the sex ratio depending on number of times queen has mated then they must have some cue to indicate degree of relatedness. 2. Ants have organic compounds (hydrocarbons) in wax layer of cuticle that could act as olfactory cue. a. If queen only mated once all workers would have similar hydrocarbon profile; if queen mated multiply workers could use amount of variation in hydrocarbon profiles to determine degree of sex bias. 3. Boomsma et al (2003) found correlation between variation in hydrocarbon profile and sex ratio in colonies with multiply mated queens. a. But when queen mated with two males with similar hydrocarbon profile workers vary little in smell and didn t bias sex ratio. b. Animals may not behave as expected due to information or other constraints Mechanisms of sex ratio conflict 1. Workers can manipulate sex ratio by neglecting or destroying males a. Sundstrom et al (1996) looked as sex ratio in the eggs and pupae of the wood ant Formica exsecta. The proportion of males decreased from eggs to pupae stages. b. This occurred in colonies where the queen had mated only once, but not in colonies where queen had mated multiply. 2. Workers can also bias sex ratio of reproductives by adjusting proportion of females that develop as queens or workers a. Example: Leptothorax acervorum
6 Mechanisms of sex ratio conflict 1. Passera et al (2001) experimentally switched queens between male-producing and female-producing colonies in red fire ants (Solenopsis invicta). 2. Sex ratio post-switch was predicted by sex ratio in colony that queen had come from. Thus, in this species, queens have control. 3. How do queens manipulate sex ratio in their favor? The queens can vary proportion of the eggs that are male. a. If few males are produced, then workers are forced to rear only female reproductives. b. If only small proportion of eggs are females, then workers will have to rear them to be workers and raise primarily male reproductives. Worker policing 1. Workers in some species can lay unfertilized eggs, which develop into drones. 2. Degree of conflict between workers of whether to rear their sister s sons or destroy the eggs will depend on how many times queen mated. a. If queen has mated multiply sisters will only be related on average by If queen has mated multiply: a. Queen prefers her sons to her grandsons produced by workers (r = 0.5>0.25). b. Laying worker prefers her sons to her brothers (r = 0.5>0.25) c. Other workers prefer brothers to nephews (r = 0.25>0.125) 4. Workers prefer queen-produced males to sister-produced males and worker eggs suppressed not only by queen but by other workers as well. Worker policing 1. Ratnieks and Visscher (1989) found evidence of worker policing in honeybees (queens mate with males during nuptial flight). 2. Introduced male eggs that had been laid by either queen or worker into colonies. 3. Worker-laid eggs removed and eaten but queen-laid eggs not. 4. Queen was excluded from cells with introduced egg so only worker bees responsible for destroying eggs. Worker policing 1. In instances of queens mating only once, workers are predicted to prefer their sister s sons produced by a worker to their brothers produced by the queen (r = 0.375>0.25). 2. Comparative study of 48 species of ants, bees and wasps found worker policing to be more common in species where queens had a greater mating frequency. a. Increases in relatedness the sons of workers vs queens resulted in decreases in policing.
7 Worker policing 1. Likelihood of eggs being destroyed by other workers reduces relative benefit of producing sons. a. Should instead invest time and resources into helping rear brothers. 2. Wenseleers and Ratnieks (2006) examined the effectiveness of policing in 10 bee and wasp species where workers produce eggs. a. Negative correlation between proportion of workers that produce eggs and effectiveness of policing. 3. Worker policing can be effective way to enforce altruism because it decreases the cost of cooperation 4. Different factors for evolution and maintenance of behaviors a. Eusociality initially involved in species with monogamous queens, which don t need policing by workers. b. When multiple matings arose worker policing ensured workers maximized genetic contribution to future generation Superorganisms 1. Different members of a colony appear to behave largely for the good of the colony as a whole, similar to different cells in a body acting for the good of the individual a. But this sounds like selection acting on the level of the colony and not individuals within the colony 2. Gardner and Grafen (2009) proposed that natural selection would lead to individuals behaving in a way that maximized the fitness of the colony when: a. Relatedness within colonies was sufficiently high (as in monogamous queens). b. Policing by workers so effective that it removes any benefit of selfish behaviors, such as worker reproduction. 3. Behaving for the good of the colony can be selected for under restrictive conditions, but unlikely to be a general evolutionary principle. In general, individuals should maximize their inclusive fitness. Comparison of vertebrates and insects 1. With possible exception of naked and Damaraland mole-rats there are no known examples of sterile castes in vertebrates 2. But in over 200 species of birds and 120 species of mammals some individuals spend part or all of their lives helping others to reproduce 3. Two main categories: a. Helpers at the nest (subsocial): 80% of birds and mammals with helpers. Group consists of breeding pair and one or more younger individuals that help with various aspects of parental care. Helpers may occasionally breed. b. Plural breeders (parasocial): several males and females share a nest and raise a communal brood. Often some individuals produce a disproportionately large share of the young 4. If subordinates not related to breeders, may be willing to help to increase likelihood of inheriting dominant, breeder rank at a later time. Helping in vertebrates 1. Groove-billed anis (Crotophaga sulcirostris) live in a territory defended by 1-4 monogamous breeding pairs 2. Group builds a communal nest in which all females lay some eggs and all group members contribute parental care 3. Not all eggs laid survive to be incubated and females compete to make sure their eggs are the ones that survive 4. Females will roll each other s eggs out of the nest. A female will stop rolling eggs out of the nest once she has started to lay her own (can t recognize their own eggs) 5. Subordinate females lay first with the dominant female laying last
8 Helping in vertebrates 6. Subordinates use several tactics to increase their chance of egg survival (laying more, produce a late egg, waiting longer between each egg) 7. But the dominant female still has the greatest number of surviving eggs (and also provides the least amount of parental care) Helping in vertebrates 1. Acorn woodpeckers live in groups of up to 15 individuals with two male and two female breeders. 2. Groups are often formed by a band of brothers and a group of sisters from a different family coming together so all the offspring are either directly or indirectly related to breeders. 3. The first female to begin laying is susceptible to having her eggs removed by the other female. a. Instead of just tossing the eggs out as with the groove-billed anis, the female will peck the egg open and the whole group will consume the contents. Helping in vertebrates 4. Acorn woodpeckers store a large supply of nuts in a granary, which consists of thousands of holes drilled into a tree 5. The difficulty of constructing and maintaining granaries is probably a strong ecological constraint that prevents young woodpeckers from leaving home and leads to communal nesting 31 Comparison of vertebrates and insects 1. Despite similarities there are also differences 2. Lifetime monogamy is rare in vertebrates so successive generations become less related to helpers a. Cooperation in long-tailed tits is only favored when attempts to breed independently fail (little to lose by helping) b. Female Seychelles warblers are more likely to help only if the they were raised by the same female 3. Female promiscuity reduces benefit of cooperating a. In comparative study of 267 bird species found that cooperative breeding less likely in species with high levels of promiscuity and within cooperative breeding species helping is less common in more promiscuous species a b Cooperative nests (%) Promiscuity (%) Cooperative Non-cooperative Breeding system Promiscuity (%) 80
9 Comparison of vertebrates and insects 1. Ecological factors thought to favor eusociality in insects (life insurance and fortress defense) less important in vertebrates. 2. Mortality rates relatively low during period it takes to rear a brood for vertebrates so benefits of cooperation lower. 3. Many vertebrate species with helpers don t live in protected areas where food is obtained but have to range over a wide area to find it (Meerkats, Seychelles warblers). Need to defend a home territory not as great. 4. Lack of available breeding territories or low chance of successful reproduction favors helping in many vertebrates. Summary 1. Sterile workers in social insects never have offspring but help rear younger siblings. This appears to go against natural selection favoring maximum efficiency at passing on genes, but degree of relatedness predisposes them to be altruistic 2. Haplodiploidy initially seemed to favor evolution of eusociality but monogamy more likely factor. 3. Life insurance and fortress defense most important ecological factors favoring eusociality. 4. Haplodiploidy results in conflict over sex ratio of reproductives and who should produce males. Workers usually win the sex ratio conflict and number of matings by queen influences conflict over who should produce males. 5. Cooperation in insects and vertebrates shows similarities (subsocial route, nest defense, provisioning of young, effect of promiscuity) as well as differences (lack of lifetime monogamy and different ecological factors).
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