Genetic determination of the queen caste in an ant hybrid zone

Julian, Glennis E.; Fewell, Jennifer H.; Gadau, Jürgen; Johnson, Robert A.; Larrabee, Debbie

doi:10.1073/pnas.112222099

Cited by 143 publications

(177 citation statements)

References 25 publications

(20 reference statements)

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“…Thus, genotypic variability does not appear as a necessary condition for intracolonial diversity and task specialization in C. cursor. This contrasts with the several cases where genetic variability among workers has been shown to influence division of labour in insect societies (honeybee: Frumhoff & Baker 1988;Robinson & Page 1988;Fuchs & Schade 1994;Page et al 1995;Kryger et al 2000;termites: Goodisman & Crozier 2003;ants: Stuart & Page 1991;Snyder 1992;Blatrix et al 2000;Julian et al 2002;Bargum et al 2004;Schwander et al 2005). The lack of genetic polyethism in C. cursor also suggests that within-colony genetic diversity is not associated with increased task efficiency and/or colony performance in this species.…”

Section: Discussioncontrasting

confidence: 46%

“…For instance, workers belonging to certain patrilines show a higher tendency to perform certain tasks such as foraging, recruiting, guarding, stinging, or nest-cleaning in the honeybee (Frumhoff & Baker 1988;Robinson & Page 1988, 1989Page et al 1989Page et al , 1995Oldroyd et al 1994), wasps (O'Donnell 1998), and in a few ant species (Stuart & Page 1991;Hughes et al 2003). Similarly, a significant genetic component to division of labour has been reported in ant colonies headed by multiple queens (polygyny), with workers belonging to different matrilines showing a different propensity to perform distinct tasks (Snyder 1992;Blatrix et al 2000;Julian et al 2002).…”

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confidence: 99%

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Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

et al. 2008

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Understanding the adaptive significance of multiple mating (polyandry) by females has long been a challenge in evolutionary biology. Several genetic and nongenetic benefits have been proposed to explain the evolution and maintenance of polyandry. In eusocial Hymenoptera, a prominent hypothesis is that increased genetic diversity within colonies results in more polymorphic workers and facilitates division of labour. We analysed the genetic basis of worker size (i.e. worker head width) and task preference in Cataglyphis cursor, an ant showing natural variations in queen-mating frequency. Our data show that increased genetic diversity within colonies does not result in more polymorphic workers. Moreover, worker head width is not different between patrilines within colonies. Consistent with these findings, worker size has a low heritable component. Moreover, task performance is not correlated with patriline. By contrast, it is significantly associated with worker size: the first foragers leaving the nest at sunrise are significantly larger than workers remaining in the nest. Overall, these results do not support the hypothesis that multiple mating is favoured because increased genetic diversity within colonies translates into more polymorphic workers and facilitates genetic polyethism. We discuss other hypotheses to account for the evolution of polyandry in C. cursor.

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Section: Discussioncontrasting

confidence: 46%

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confidence: 99%

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

et al. 2008

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“…Hung & Vinson 1977;Ross et al 1987;Vander Meer & Lofgren 1989;Helms Cahan & Vinson 2003;Shoemaker et al 2006) and several other ant genera (Lasius : Pearson 1983b, Seifert 1999, Umphrey 2006Formica: Seifert 1999, Seifert & Goropashnaya 2004Temnothorax: Douwes & Stille 1991, Seifert 1999, Pusch et al 2006aPogonomyrmex: Helms Cahan et al 2002, Julian et al 2002, Schwander et al 2007bCrematogaster: Feldhaar et al 2003, H. Feldhaar 2006. It appears that in some areas of Central Europe, almost half of all female sexuals of the well-studied and highly diverse ant genus Temnothorax mate with allospecific males (Douwes & Stille 1991;Seifert 1999).…”

Section: Seemingly Indiscriminate Mating and The Commonness Of Hybridmentioning

confidence: 99%

“…These lineages are reproductively isolated from the pure parental species and obligately hybridize. Sterile workers are produced from interlineage zygotes, while female sexuals are raised from eggs fertilized by sperm from the same lineage (Helms Cahan et al 2002Julian et al 2002;Volny & Gordon 2002;Helms Cahan & Keller 2003;Anderson et al 2006), resulting in a reproductive division of labour between hybrid workers and purelineage female sexual. This mechanism of caste determination appears to be genetically fixed, as (2006a,b) a Hybridization between the respective species was detected with: A, allozyme data; mtDNA, mitochondrial DNA; nDNA, nuclear DNA including microsatellite data; M, morphological data.…”

Section: Individual-and Species-level Consequences Of Hybridization Imentioning

confidence: 99%

Lifelong commitment to the wrong partner: hybridization in ants

Feldhaar

Foitzik

Heınze

2008

Phil. Trans. R. Soc. B

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The extraordinary lifelong partner commitment in social insects is expected to increase choosiness in both sexes and therefore to be associated with particularly low hybridization frequencies. Yet, more and more studies reveal that in many ant taxa hybrids are surprisingly common, with up to half of all female sexuals receiving sperm from allospecific males in extreme cases. In a few ant species, hybridization has led to the evolution of reproductively isolated new lineages with a bizarre system of genetic caste differentiation: colonies produce hybrid workers and pure-lineage female sexuals. This requires that colonies either contain multiple queens or that queens mate multiple times. In most other cases, hybridization appears to be an evolutionary dead end and fertile hybrid queens are rarely found. In such cases, haplodiploid sex determination appears to decrease the costs of mating with an allospecific male. As long as hybrid workers are viable, a cross-mated queen can partially rescue its fitness by producing males from unfertilized eggs. Mating with an allospecific partner may thus be an option for queens when conspecific mates are not available. The morphological similarity of most ant males, perhaps resulting from the lack of sexual conflict, may similarly contribute to the commonness of hybridization.

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“…In GCD colonies, gynes are consistently homozygous at diagnostic loci whereas workers are heterozygous at the same loci (12,16,17). This genetic colony structure occurs because founding queens mate with males of two distinct and reproductively isolated lineages, producing heterozygous workers from alternate-lineage matings and homozygous gynes from same-lineage matings.…”

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confidence: 99%

Population-wide lineage frequencies predict genetic load in the seed-harvester antPogonomyrmex

Anderson

Hölldobler²,

Fewell

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Many populations of the seed-harvester ant Pogonomyrmex barbatus exhibit genetic caste determination (GCD) generated by the interbreeding of two distinct yet interdependent lineages. Samelineage matings are genetically predestined to become female reproductives (gynes) whereas alternate-lineage matings become workers. The perpetuation of this system requires that reproductives of both lineages are available for mating and are thus part of the effective population. We label these dependent lineage populations, because each lineage depends on the alternate lineage for worker production. Here we investigate the potential costs associated with GCD in a population with highly skewed lineage frequencies. We reared colonies using newly mated queens from a GCD population and an ecologically equivalent Pogonomyrmex rugosus population with environmental caste determination. GCD founding queens suffer a genetic load from mating randomly and produce fewer brood with advanced development compared with environmental caste determination queens. Our results indicate that GCD queens acquiring a high proportion of same-lineage sperm are unlikely to found a colony successfully. Given model parameters of random mating and founding queens mating with three males on average, there was a close fit between theoretical expectations of variation in colony worker production based on mating and lineage frequencies and empirical deficits in worker production. As expected, severely decreased worker production was specific to the common lineage, suggesting that negative frequency-dependent selection acts to stabilize a dependent lineage system. genetic caste determination ͉ dependent lineage system ͉ frequency-dependent selection ͉ mating frequency ͉ obligate polyandry T he success of social insect societies is largely attributed to reproductive division of labor in which most colony members are sterile and provide for the reproductive caste, rather than producing their own progeny (1). The accepted mechanism for differentiation of colony members into reproductive and sterile castes is environmental caste determination (ECD), or caste polyphenism, a developmentally plastic process in which eggs or larvae of similar genotypes develop into discrete phenotypes depending on their environment (2-6). Genetic caste determination (GCD) occurs when different female genotypes are more likely to become either reproductives (gynes) or workers. Gynes become queens when they successfully mate and found a new colony. Although ECD is clearly predominant, there is growing evidence for a genetic influence on caste determination in some Hymenoptera (7-11).Differentiation of gynes and workers is determined by genotype in many populations of the seed-harvester ants Pogonomyrmex barbatus and Pogonomyrmex rugosus (12-15). In GCD colonies, gynes are consistently homozygous at diagnostic loci whereas workers are heterozygous at the same loci (12,16,17). This genetic colony structure occurs because founding queens mate with males of two distinct and reproductively iso...

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Genetic determination of the queen caste in an ant hybrid zone

Cited by 143 publications

References 25 publications

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

Lifelong commitment to the wrong partner: hybridization in ants

Population-wide lineage frequencies predict genetic load in the seed-harvester antPogonomyrmex

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