Evolution of eusociality

Last updated
Honeybee workers collaborating on a comb have given up their ability to reproduce, an extreme expression of eusocial behavior. Todd Huffman - Lattice (by).jpg
Honeybee workers collaborating on a comb have given up their ability to reproduce, an extreme expression of eusocial behavior.

Eusociality evolved repeatedly in different orders of animals, notably termites and the Hymenoptera (the wasps, bees, and ants). This 'true sociality' in animals, in which sterile individuals work to further the reproductive success of others, is found in termites, ambrosia beetles, gall-dwelling aphids, thrips, marine sponge-dwelling shrimp ( Synalpheus regalis ), naked mole-rats (Heterocephalus glaber), and many genera in the insect order Hymenoptera. [1] The fact that eusociality has evolved so often in the Hymenoptera (between 8 and 11 times [2] ), but remains rare throughout the rest of the animal kingdom, has made its evolution a topic of debate among evolutionary biologists. Eusocial organisms at first appear to behave in stark contrast with simple interpretations of Darwinian evolution: passing on one's genes to the next generation, or fitness, is a central idea in evolutionary biology.

Contents

Current theories propose that the evolution of eusociality occurred either due to kin selection, proposed by W. D. Hamilton, [3] or by the competing theory of multilevel selection as proposed by E.O. Wilson and colleagues. [4] No single trait or model is sufficient to explain the evolution of eusociality, and most likely the pathway to eusociality involved a combination of pre-conditions, ecological factors, and genetic influences.

Overview of eusociality

Eusociality can be characterized by four main criteria: overlapping generations, cooperative brood care, philopatry, and reproductive altruism. [5] Overlapping generations means that multiple generations live together, and that older offspring may help the parents raise their siblings. Cooperative brood care is when individuals other than the parents assist in raising the offspring through means such as food gathering and protection. Philopatry is when individuals remain living in their birthplace.

The final category, reproductive altruism, is the most divergent from other social orders. Altruism occurs when an individual performs a behavior that benefits a recipient in some way, but at the individual's own expense. [3] Reproductive altruism is one of the most extreme forms of altruism. This is when most members of the group give up their own breeding opportunities in order to participate in the reproductive success of other individuals. [5] The individuals giving up their own reproductive success form a sterile caste of workers within the group. All species that practice reproductive altruism produce one or more queens, the only breeding females, who are larger than the rest. The remainder of the society is composed of a few breeding males, sterile male and female workers, and the young. [5]

Early hypotheses

Charles Darwin considered the evolution of eusociality a major problem for his theory of natural selection. In The Origin of Species , he described the existence of sterile worker castes in the social insects as "the one special difficulty, which at first appeared to me insuperable and actually fatal to my whole theory". In the next paragraph of his book, Darwin describes a solution. If the trait of sterility can be carried by some individuals without expression, and those individuals that do express sterility help reproductive relatives, the sterile trait can persist and evolve. [6]

Darwin was on the right track, except sterility is not a characteristic shared among all eusocial animals. Sterile workers of many eusocial species are not actually physiologically sterile. Male workers can still produce sperm, and female workers sometimes lay eggs, and in some species, become the new queen if the old one dies (observed in Hymenoptera, termites, and shrimp). [1] [5]

This insight led to inclusive fitness and kin selection becoming important theories during the 20th century to help explain eusociality. Inclusive fitness is described as a combination of one's own reproductive success and the reproductive success of others that share similar genes. [1] Animals may increase their inclusive fitness through kin selection. Kin selection is when individuals help close relatives with their reproduction process, seemingly because relatives will propagate some of the individual's own genes. Kin selection follows Hamilton's Rule, which suggests that if the benefit of a behavior to a recipient, taking into account the genetic relatedness of the recipient to the altruist, outweighs the costs of the behavior to the altruist, then it is in the altruist's genetic advantage to perform the altruistic behavior. [3]

Current theories

Haplodiploidy/Kin selection

William D. Hamilton proposed that eusociality arose in social Hymenoptera by kin selection because of their interesting genetic sex determination trait of haplodiploidy. Because males are produced by parthenogenesis (they come from unfertilized eggs and thus only have one set of chromosomes), and females are produced from fertilized eggs, sisters from a singly-mated mother share (on average) 75% of their genes, whereas mothers always share only 50% of their genes with their offspring. Thus, sisters will propagate their own genes more by helping their mothers to raise more sisters, than to leave the nest and raise their own daughters. [3]

Though Hamilton's argument appears to work well for Hymenoptera, it excludes diploid eusocial organisms (inter-sibling relatedness ≤ parent-offspring relatedness = 0.5). Even in haplodiploid systems, the average relatedness between sisters falls off rapidly when a queen mates with multiple males (r=0.5 for 2 mates, and even lower for more). Moreover, males share only 25% of their sisters' genes, and, in cases of equal sex ratios, females are related to their siblings on average by 0.5 which is no better than raising their own offspring. [7] However, despite the shortcomings of the haplodiploidy hypothesis, it is still considered to have some importance. For example, many bees have female-biased sex ratios and/or invest less in or kill males. Analysis has shown that in Hymenoptera, the ancestral female was monogamous in each of the eight independent cases where eusociality evolved. [2] This indicates that the high relatedness between sisters favored the evolution of eusociality during the initial stages on several occasions. This helps explain the abundance of eusocial genera within the order Hymenoptera, including three separate origins within halictid bees alone. [8]

Monogamy

The monogamy hypothesis, formulated by Jacobus Boomsma in 2007, is currently the leading hypothesis concerning the initial evolution of eusociality in the Hymenoptera. It uses Hamilton's kin selection approach in a way that applies to both haploid and diploid organisms. If a queen is lifetime-strictly monogamous - in other words, she mates with only one individual during her entire life - her progeny will be equally related to their siblings and to their own offspring (r=0.5 in both cases - this is an average of sisters [0.75] and brothers [0.25]). Thus, natural selection will favor cooperation in any situation where it is more efficient to raise siblings than offspring, and this could start paving a path towards eusociality. This higher efficiency becomes especially pronounced after group living evolves. [9] [10]

In many monogamous animals, an individual's death prompts its partner to look for a new mate, which would affect relatedness and hinder the evolution of eusociality: workers would be much more related to their offspring than their siblings. However, many Hymenoptera have a form of lifetime monogamy in which the queen mates with a single male, who then dies before colony founding. This seems to be the ancestral state in all Hymenopteran lineages that have evolved eusociality. [2] Most termites also have a mating system in which a reproductive female (the queen) commits to a single male for life (the king), and this pattern seems to be ancestral in termites. [9] Lastly, strict monogamy facilitated eusociality in the sponge-dwelling shrimp. [11]

Inbreeding

In species where philopatry predominates, and there are few emigrants to the nest, intense inbreeding can occur, as is the case in eusocial species. Inbreeding can mimic and even surpass the effects of haplodiploidy. Siblings may actually share greater than 75% of their genes. Like in haplodiploidy kin selection, the individuals can propagate their own genes more through the promotion of more siblings, rather than their own offspring. [1] [5] For example, the need for dispersal and aggregation of multiclonal groups may have helped to drive the evolution of eusociality in aphids. [12]

Termites

In termites, two additional hypotheses have been proposed. The first is the Chromosomal Linkage Hypothesis, where much of the termite genome is sex-linked. This makes sisters related somewhat above 50%, and brothers somewhat above 50%, but brother-sister relatedness less than 50%. Termite workers might then bias their cooperative brood care towards their own sex. This hypothesis also mimics the effects of haplodiploidy, but proposes that males would help raise only the queen's male offspring, while females would only care for the queen's female offspring. [13]

The symbiont hypothesis in termites is quite different from the others. With each molt, termites lose the lining of their hindgut and the subsequent bacteria and protozoa that colonize their guts for cellulose digestion. They depend on interactions with other termites for their gut to be recolonized, thus forcing them to become social. This could be a precursor, or pre-condition for why eusociality evolved in termites. [13]

Pre-conditions

The accumulation of certain traits may serve as "pre-conditions" for the evolution of eusociality to more likely occur in certain species. Eusociality is likely to be a trait arising from convergent evolution, considering the lack of evolutionary relationships between the species that have evolved eusociality. However, eusociality is especially concentrated in the order Isoptera (termites), where all members are eusocial, most species of the Formicidae family (ants), and multiple species of the superfamily Apoidea (bees and wasps). [14] Although the symbiont hypothesis serves as a pre-condition for termites to evolve into eusocial societies, scientists have found two crucial pre-conditions for the evolution of eusociality across all species. These include: 1. Altricial offspring (require large amounts of parental care to reach maturity); 2. Low reproductive success rates of solitary pairs that attempt to reproduce. [1] These pre-conditions led to the two lifestyle characteristics that are observed in all eusocial species: nest building and extensive parental care. Experimental evidence for this can be seen in certain studies where species from genus of solitary bees, such as Lasioglossum, may behave like eusocial bees with the division of labor when forced together experimentally. [15] [16] In the case of termites, as recent phylogenetic studies have showed them being closely related to wood-eating cockroaches (genus Cryptocercus), [17] which are subsocial and engage in biparental care, their eusocialty may have evolved from subsocialty. [18]

Ecological factors

Ecological factors were also probably a precursor to eusociality. [19] [20] For example, the sponge-dwelling shrimp depend upon the sponge's feeding current for food, termites depend upon dead, decaying wood, and naked mole rats depend upon tubers in the ground. [5] [13] [21] Each of these resources has patchy distributions throughout the environments of these animals. This means there is a high cost to dispersing (individual may not find another source before it starves), and these resources must be defended for the group to survive. These requirements make it a necessity to have high social order for the survival of the group. [5] [21]

Genetic influences

Genetic constraints may have influenced the evolution of eusociality. The genome structure of the order Hymenoptera has been found to have the highest recombination rates of any other groups in Animalia. The eusocial genus Apis , the honeybees, have the highest recombination rate in higher eukaryotes. [22] [23] Genes determining worker behavior and division of labor have been found in regions of the Apis genome with the highest rates of recombination and molecular evolution. [22] These mechanisms are likely important to the evolution of eusociality because high recombination rates are associated with the creation of novel genes, upon which natural selection can act. [23] This could have been important in other eusocial genera. Biased gene conversion rates are also higher in eusocial species. [22] This could increase genotypic diversity, which could allow workers to meet the demands of a changing social structure more easily. [23] Another hypothesis is that the lower overall genetic diversity as eusociality levels increase throughout the family Apidaeis due to a decreased exposure to parasites and pathogens. [24] [25]

Mechanisms

Manipulation

Eusociality appears to be maintained through manipulation of the sterile workers by the queen. [1] The mechanisms for this include hormonal control through pheromones, restricting food to young in order to control their size, consumption of any eggs laid by females other than the queen, and behavioral dominance. In naked mole rats, this behavioral dominance occurs in the form of the queen facing the worker head-to-head, and shoving it throughout the tunnels of the naked mole rats' burrow for quite a distance. [5]

Group selection

Nowak, et al. (2010) outlines a path by which eusociality could evolve by means of multi-level (group) selection in five steps: [4]

  1. Formation of groups: Groups could consist of parent-offspring groups or unrelated groups (in situations where cooperation is beneficial) living in a structured nest.
  2. Pre-adaptations: Pre-adaptations for social living, such as progressive provisioning, will push the group further toward eusociality.
  3. Mutations: Mutations will arise and be selected. Some genes are known to have been silenced in social insect history, leading to the reduction of dispersal behavior and the origin of the wingless caste.
  4. Natural Selection Acts on Emergent Traits: The interactions of the individuals can be considered as part of the extended phenotype of the queen. These interactions produce emergent properties upon which natural selection can act.
  5. Multi-level selection: More cooperative groups out-compete less cooperative groups.

Nowak's paper, however, received major criticisms for erroneously separating inclusive fitness theory from "standard natural selection". Over 150 authors replied [26] arguing that Nowak, et al. misrepresent 40 years of empirical literature.

Related Research Articles

<span class="mw-page-title-main">Hymenoptera</span> Order of insects comprising sawflies, wasps, bees, and ants

Hymenoptera is a large order of insects, comprising the sawflies, wasps, bees, and ants. Over 150,000 living species of Hymenoptera have been described, in addition to over 2,000 extinct ones. Many of the species are parasitic. Females typically have a special ovipositor for inserting eggs into hosts or places that are otherwise inaccessible. This ovipositor is often modified into a stinger. The young develop through holometabolism —that is, they have a wormlike larval stage and an inactive pupal stage before they reach adulthood.

<span class="mw-page-title-main">Kin selection</span> Evolutionary strategy favoring relatives

Kin selection is a process whereby natural selection favours a trait due to its positive effects on the reproductive success of an organism's relatives, even when at a cost to the organism's own survival and reproduction. Kin selection can lead to the evolution of altruistic behaviour. It is related to inclusive fitness, which combines the number of offspring produced with the number an individual can ensure the production of by supporting others. A broader definition of kin selection includes selection acting on interactions between individuals who share a gene of interest even if the gene is not shared due to common ancestry.

<span class="mw-page-title-main">Trophallaxis</span> Transfer of food between members of a community through stomodeal or proctodeal means

Trophallaxis is the transfer of food or other fluids among members of a community through mouth-to-mouth (stomodeal) or anus-to-mouth (proctodeal) feeding. Along with nutrients, trophallaxis can involve the transfer of molecules such as pheromones, organisms such as symbionts, and information to serve as a form of communication. Trophallaxis is used by some birds, gray wolves, vampire bats, and is most highly developed in eusocial insects such as ants, wasps, bees, and termites.

<span class="mw-page-title-main">Behavioral ecology</span> Study of the evolutionary basis for animal behavior due to ecological pressures

Behavioral ecology, also spelled behavioural ecology, is the study of the evolutionary basis for animal behavior due to ecological pressures. Behavioral ecology emerged from ethology after Niko Tinbergen outlined four questions to address when studying animal behaviors: What are the proximate causes, ontogeny, survival value, and phylogeny of a behavior?

<span class="mw-page-title-main">Group selection</span> Proposed mechanism of evolution

Group selection is a proposed mechanism of evolution in which natural selection acts at the level of the group, instead of at the level of the individual or gene.

In evolutionary biology, inclusive fitness is one of two metrics of evolutionary success as defined by W. D. Hamilton in 1964:

<span class="mw-page-title-main">Altruism (biology)</span> Behaviour that increases the fitness of another while decreasing the fitness of self

In biology, altruism refers to behaviour by an individual that increases the fitness of another individual while decreasing their own. Altruism in this sense is different from the philosophical concept of altruism, in which an action would only be called "altruistic" if it was done with the conscious intention of helping another. In the behavioural sense, there is no such requirement. As such, it is not evaluated in moral terms—it is the consequences of an action for reproductive fitness that determine whether the action is considered altruistic, not the intentions, if any, with which the action is performed.

<span class="mw-page-title-main">Blattodea</span> Order of insects that includes cockroaches and termites

Blattodea is an order of insects that contains cockroaches and termites. Formerly, termites were considered a separate order, Isoptera, but genetic and molecular evidence suggests they evolved from within the cockroach lineage, cladistically making them cockroaches as well. The Blattodea and the mantis are now all considered part of the superorder Dictyoptera. Blattodea includes approximately 4,400 species of cockroach in almost 500 genera, and about 3,000 species of termite in around 300 genera.

<span class="mw-page-title-main">Haplodiploidy</span> Biological system where sex is determined by the number of sets of chromosomes

Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. Haplodiploidy is sometimes called arrhenotoky.

<span class="mw-page-title-main">Sociality</span> Form of collective animal behaviour

Sociality is the degree to which individuals in an animal population tend to associate in social groups (gregariousness) and form cooperative societies.

The concept of the evolution of morality refers to the emergence of human moral behavior over the course of human evolution. Morality can be defined as a system of ideas about right and wrong conduct. In everyday life, morality is typically associated with human behavior rather than animal behavior. The emerging fields of evolutionary biology, and in particular evolutionary psychology, have argued that, despite the complexity of human social behaviors, the precursors of human morality can be traced to the behaviors of many other social animals. Sociobiological explanations of human behavior remain controversial. Social scientists have traditionally viewed morality as a construct, and thus as culturally relative, although others such as Sam Harris argue that there is an objective science of morality.

<span class="mw-page-title-main">Eusociality</span> Highest level of animal sociality a species can attain

Eusociality is the highest level of organization of sociality. It is defined by the following characteristics: cooperative brood care, overlapping generations within a colony of adults, and a division of labor into reproductive and non-reproductive groups. The division of labor creates specialized behavioral groups within an animal society, sometimes called castes. Eusociality is distinguished from all other social systems because individuals of at least one caste usually lose the ability to perform behaviors characteristic of individuals in another caste. Eusocial colonies can be viewed as superorganisms.

<i>Nasutitermes corniger</i> Species of termite

Nasutitermes corniger is a species of arboreal termite that is endemic to the neotropics. It is very closely related to Nasutitermes ephratae. The species has been studied relatively intensively, particularly on Barro Colorado Island, Panama. These studies and others have shown that the termite interacts with many different organisms including a bat that roosts in its nest and various species of ants that cohabit with the termite.

<i>Austroplatypus incompertus</i> Species of beetle

Austroplatypus incompertus, a type of ambrosia beetle, is endemic to Australia. They are found in mesic forests, and subtropical and tropical ecosystems along the east coast of Australia. There are many unique characteristics attributable to the A. incompertus, like their gallery excavation in several Eucalyptus species, their obligate eusocial behavior, their relationship with fungi, and their unique sexual dimorphism. These beetles are one of the only insects that display obligate eusocial behavior. Additionally, their sexually dimorphic traits are of interest, since body size is reversed with males having smaller torsos than female A. incompertus beetles.

<span class="mw-page-title-main">Halictinae</span> Subfamily of bees

Within the insect order Hymenoptera, the Halictinae are the largest, most diverse, and most recently diverged of the four halictid subfamilies. They comprise over 2400 bee species belonging to the five taxonomic tribes Augochlorini, Thrinchostomini, Caenohalictini, Sphecodini, and Halictini, which some entomologists alternatively organize into the two tribes Augochlorini and Halictini.

<i>Lasioglossum zephyrus</i> Species of bee

Lasioglossum zephyrus is a sweat bee of the family Halictidae, found in the U.S. and Canada. It appears in the literature primarily under the misspelling "zephyrum". It is considered a primitively eusocial bee, although it may be facultatively solitary. The species nests in burrows in the soil.

Synalpheus regalis is a species of snapping shrimp that commonly live in sponges in the coral reefs along the tropical West Atlantic. They form a prominent component of the diverse marine cryptofauna of the region. For the span of their entire lives, they live in the internal canals of the host sponge, using it as a food resource and shelter. It has been shown that colonies contain over 300 individuals, but only one reproductive female. Also, larger colony members, most of which apparently never breed, defend the colony against heterospecific intruders. This evidence points towards the first known case of eusociality in a marine animal.

<span class="mw-page-title-main">Worker policing</span> Insects destroying eggs not laid by queen

Worker policing is a behavior seen in colonies of social hymenopterans whereby worker females eat or remove eggs that have been laid by other workers rather than those laid by a queen. Worker policing ensures that the offspring of the queen will predominate in the group. In certain species of bees, ants and wasps, workers or the queen may also act aggressively towards fertile workers. Worker policing has been suggested as a form of coercion to promote the evolution of altruistic behavior in eusocial insect societies.

<i>Kladothrips</i> Genus of thrips

Kladothrips is a genus of Australian gall thrips. It is notable for including some of the few organisms outside of Hymenoptera that exhibit eusociality.

<i>Halictus sexcinctus</i> Species of bee

Halictus sexcinctus, commonly referred to as the six-banded furrow bee, is a species of sweat bee found throughout Europe and as far east as Asian Turkey and Iraq. The H. sexcinctus can be easily confused with the closely related species, Halictus scabiosae, due to very similar morphological features. H. sexcinctus show a social polymorphism in which different colonies can exhibit solitary, communal, or eusocial structure. Due to this large variance in social organization, it was suspected that it was not one species at all, but rather multiple, cryptic species. However, genetic analysis was able to confirm these varying populations as one species. H. sexcinctus will forage from multiple flower species, but prefers plant species with wide-open flowers. Their nests can be found dug into the ground in loamy or sandy soil.

References

  1. 1 2 3 4 5 6 Andersson, M. (1984). "Evolution of eusociality". Annu. Rev. Ecol. Syst. 15 (1): 165–189. Bibcode:1984AnRES..15..165A. doi:10.1146/annurev.es.15.110184.001121.
  2. 1 2 3 Hughes, W. O. H.; Oldroyd, B. P.; Beekman, M.; Ratnieks, F. L. W. (2008). "Ancestral Monogamy Shows Kin Selection is Key to the Evolution of Eusociality". Science. 320 (5880): 1213–1216. Bibcode:2008Sci...320.1213H. doi:10.1126/science.1156108. PMID   18511689. S2CID   20388889.
  3. 1 2 3 4 Hamilton, W. D. (1964). "The genetical theory of social behaviour, I, II". Journal of Theoretical Biology. 7 (1): 1–52. Bibcode:1964JThBi...7....1H. doi:10.1016/0022-5193(64)90038-4. PMID   5875341.
  4. 1 2 Nowak; et al. (2010). "The evolution of eusociality". Nature. 466 (7310): 1057–1062. Bibcode:2010Natur.466.1057N. doi:10.1038/nature09205. PMC   3279739 . PMID   20740005.
  5. 1 2 3 4 5 6 7 8 Honeycutt, R (1992). "Naked mole-rats". American Scientist. 80 (1): 43–53. Bibcode:1992AmSci..80...43H.
  6. ↑ Darwin, C. (1859) On the Origin of Species by Means of Natural Selection or The Preservation of Favored Races in the Struggle for Life. John Murray.
  7. ↑ Foster, K.; Wenseleers, T.; Ratnieks, F. (2006). "Kin selection is the key to altruism". Trends in Ecology & Evolution. 21 (2): 57–60. Bibcode:2006TEcoE..21...57F. doi:10.1016/j.tree.2005.11.020. PMID   16701471.
  8. ↑ Danforth, Bryan (October 29, 2001). "Evolution of sociality in a primitively eusocial lineage of bees". Proceedings of the National Academy of Sciences. 99 (1): 286–290. Bibcode:2002PNAS...99..286D. doi: 10.1073/pnas.012387999 . PMC   117553 . PMID   11782550.
  9. 1 2 Boomsma, J. (2007). "Kin selection versus sexual selection: why the ends do not meet". Current Biology. 17 (16): R673–R683. Bibcode:2007CBio...17.R673B. doi: 10.1016/j.cub.2007.06.033 . PMID   17714661. S2CID   886746.
  10. ↑ Boomsma, J. (2009). "Lifetime monogamy and the evolution of eusociality". Phil. Trans. R. Soc. B. 364 (1533): 3191–3208. doi:10.1098/rstb.2009.0101. PMC   2781870 . PMID   19805427.
  11. ↑ Duff, J. E.; Macdonald, K. S. (2010). "Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis". Proceedings of the Royal Society B: Biological Sciences. 277 (1681): 575–584. doi:10.1098/rspb.2009.1483. PMC   2842683 . PMID   19889706.
  12. ↑ Abbot, Patrick (October 2009). "On the evolution of dispersal and altruism in aphids". Evolution. 63 (10): 2687–2696. doi:10.1111/j.1558-5646.2009.00744.x. PMID   19500147. S2CID   12865398.
  13. 1 2 3 Thorne, B (1997). "Evolution of eusociality in termites". Annu. Rev. Ecol. Syst. 28 (11): 27–54. Bibcode:1997AnRES..28...27T. doi:10.1146/annurev.ecolsys.28.1.27. PMC   349550 .
  14. ↑ Nowak, Martin A.; Tarnita, Corina E.; Wilson, Edward O. (August 2010). "The evolution of eusociality". Nature. 466 (7310): 1057–1062. Bibcode:2010Natur.466.1057N. doi:10.1038/nature09205. ISSN   0028-0836. PMC   3279739 . PMID   20740005.
  15. ↑ Wcislo, W.T. (August 1997). "Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) figueresi (Hymenoptera, Halictidae)". Insectes Sociaux. 44 (3): 199–208. doi:10.1007/s000400050041. ISSN   0020-1812.
  16. ↑ Jeanson, Raphaël; Kukuk, Penelope F.; Fewell, Jennifer H. (November 2005). "Emergence of division of labour in halictine bees: contributions of social interactions and behavioural variance". Animal Behaviour. 70 (5): 1183–1193. doi:10.1016/j.anbehav.2005.03.004. ISSN   0003-3472.
  17. ↑ DjernæS, Marie; Klass, Klaus-Dieter; Picker, Mike D.; Damgaard, Jakob (January 2012). "Phylogeny of cockroaches (Insecta, Dictyoptera, Blattodea), with placement of aberrant taxa and exploration of out-group sampling". Systematic Entomology. 37 (1): 65–83. Bibcode:2012SysEn..37...65D. doi:10.1111/j.1365-3113.2011.00598.x. ISSN   0307-6970.
  18. ↑ Klass, Klaus-Dieter; Nalepa, Christine; Lo, Nathan (2008-03-01). "Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus vs. Parasphaeria boleiriana". Molecular Phylogenetics and Evolution. 46 (3): 809–817. Bibcode:2008MolPE..46..809K. doi:10.1016/j.ympev.2007.11.028. ISSN   1055-7903. PMID   18226554.
  19. ↑ Bourke, A. F. (1999). "Colony size, social complexity and reproductive conflict in social insects". Journal of Evolutionary Biology. 12 (2): 245–257. doi: 10.1046/j.1420-9101.1999.00028.x . S2CID   85187599.
  20. ↑ Ross, L. (2013). "Ecology, Not the Genetics of Sex Determination, Determines Who Helps in Eusocial Populations". Current Biology. 23 (23): 2383–2387. Bibcode:2013CBio...23.2383R. doi: 10.1016/j.cub.2013.10.013 . PMID   24268409.
  21. 1 2 Duffy, J (1996). "Eusociality in a coral reef shrimp". Nature. 381 (6582): 512–514. Bibcode:1996Natur.381..512D. doi:10.1038/381512a0. S2CID   33166806.
  22. 1 2 3 Kent; et al. (2012). "Recombination is associated with the evolution of genome structure and worker behavior in honey bees". Proceedings of the National Academy of Sciences. 109 (44): 18012–18017. Bibcode:2012PNAS..10918012K. doi: 10.1073/pnas.1208094109 . PMC   3497793 . PMID   23071321.
  23. 1 2 3 Wilfert; et al. (2007). "Variation in genomic recombination rates among animal taxa and the case of social insects". Heredity. 98 (4): 189–197. doi: 10.1038/sj.hdy.6800950 . PMID   17389895.
  24. ↑ Kapheim; et al. (2015). "Genomic signatures of evolutionary transitions from solitary to group living". Science. 348 (6239): 1139–43. Bibcode:2015Sci...348.1139K. doi:10.1126/science.aaa4788. PMC   5471836 . PMID   25977371.
  25. ↑ Woodard; et al. (2011). "Genes involved in convergent evolution eusociality in bees". Proceedings of the National Academy of Sciences. 108 (18): 7472–7477. Bibcode:2011PNAS..108.7472W. doi: 10.1073/pnas.1103457108 . PMC   3088614 . PMID   21482769.
  26. ↑ Abbot, P.; et al. (2011). "Inclusive fitness theory and eusociality". Nature. 471 (7339): E1–E4. Bibcode:2011Natur.471E...1A. doi:10.1038/nature09831. PMC   3836173 . PMID   21430721.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.