Determinants of intracolonial relatedness in<i>Pogonomyrmex rugosus</i>(Hymenoptera; Formicidae): mating frequency and brood raids

Gadau, Jürgen; Strehl, Christoph Peter; Oettler, Jan; Hölldobler, Bert

doi:10.1046/j.1365-294x.2003.01853.x

Cited by 56 publications

(63 citation statements)

References 37 publications

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“…The fact that the majority of these colonies produce gynes on an annual basis (34) suggests they have also mated with at least one same-lineage male, and therefore the actual mating frequency is at least 1 greater than the 3.34 estimate. This conservative estimate places the mating frequency of DL P. barbatus close to the mating frequency of 4.71 established for ECD P. rugosus (35).…”

Section: Discussionsupporting

confidence: 58%

“…3), the associated P value (0.07) has marginal significance, indicating a higher mating frequency, sperm precedence, or extrinsic influences on colony founding success. Other harvester ant species, P. rugosus, Pogonomyrmex occidentalis, and Pogonomyrmex badius, show considerable variability in patriline numbers and an unequal patriline representation within colonies (11,35,36). Thus, even if a queen mates with multiple males, the sperm of a single male may be overrepresented during initial brood production.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 58%

Section: Discussionmentioning

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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“…Samples were centrifuged and the supernatant was used as the template for PCR amplification. Individuals were genotyped at eight microsatellite loci using eight primer sets: L-18 (Foitzik et al, 1997), Myrt3 (Bourke et al, 1997), PO8 (Wiernasz et al, 2004), Pb5, Pb7, Pb8, Pb10 (Volny and Gordon, 2002b) and PR-1 (Gadau et al, 2003), according to the procedure described in Helms Cahan and Keller (2003). Myrt3 and PR-1 are diagnostic for lineage.…”

Section: Identification Of Queen Genotypesmentioning

confidence: 99%

“…Number of alleles and gene diversity (Nei, 1978) are shown in Table 1. We classified queens as J1 or J2 by their genotypes at the diagnostic loci Myrt3 (Bourke et al, 1997) and PR-1 (Gadau et al, 2003). Our sample included 59 J1 colonies and 71 J2 colonies.…”

Section: Genetic Diversitymentioning

confidence: 99%

Fine-scale genetic structure and dispersal distance in the harvester ant Pogonomyrmex barbatus

Suni

Gordon

2009

Heredity

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Dispersal has important genetic and evolutionary consequences. It is notoriously difficult to study in some ant species, because reproductives fly from parent nests to mating aggregations and then to new nest sites. We used genetic techniques to measure dispersal distance and characterize patterns of genetic variation in a population of the harvester ant Pogonomyrmex barbatus. This population consists of two interdependent yet genetically distinct mitochondrial lineages, each associated with specific alleles at nuclear loci. We found moderate levels of genetic structure for both lineages and a significant pattern of isolation by distance when individual colonies were the operational unit of study. Dispersal distances calculated from the slope of the regression of genetic on geographic distance were 65.3 m for J1 and 85.8 m for J2. These results are consistent with previous observations of many mating aggregations over small geographic areas. In dependent-lineage populations like our study population, females must mate with males of the opposite lineage to produce workers, and with males of the same lineage to produce female reproductives. Because lineage ratios differ from 1:1 throughout the southwestern United States, restricted dispersal between sites with different lineage ratios could have important effects on dependent-lineage population dynamics. Our results suggest that it is unlikely that many individuals disperse from areas dominated by one lineage to areas dominated by another.

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“…Species of Pogonomyrmex are characterized by colonies headed by a single, polyandrous queen (17,(43)(44)(45). In our study population, the queens typically mate with six or seven males (46), may live for as many as…”

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confidence: 99%

Patriline shifting leads to apparent genetic caste determination in harvester ants

Wiernasz

Cole

2010

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

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The harvester ant, Pogonomyrmex occidentalis, is characterized by high levels of intracolonial genetic diversity resulting from multiple mating by the queen. Within reproductively mature colonies, the relative frequency of different male genotypes (patrilines) is not stable. The difference between samples increases with time, nearing an asymptote after a year. Patriline distributions in gynes and workers display similar patterns of change. A consequence of changing patriline distributions is that workers and gynes appear to have different fathers. However, apparent genetic differences between castes are caused by changing paternity among all females. Temporal variation in the relative frequency of patrilines may be a consequence of processes that reflect sexual conflict, such as sperm clumping. Recent work documenting genotype differences between physical castes (workers and gynes; major and minor workers) in several species of ants has been interpreted as evidence of genetic caste determination. Reanalysis of these studies found little support for this hypothesis. Apparent caste determination may result from temporal variation in sperm use, rather than from fertilization bias among male ejaculates. M orphological traits frequently display phenotypic plasticity (reviewed in refs. 1, 2); such variation is especially common in insects (3). Phenotypic plasticity generally is assumed to be responsible for physical castes in the social insects, including differences between gynes (virgin queens) and workers (nonreproductive caste) and differences between workers (major and minor worker castes). The proximal cause of the plasticity is thought to be largely nutritional (4, 5), and in some species, such as the honey bee, the underlying nutritional mechanisms are well understood (6, 7). As with any phenotype, physical caste is unlikely to be completely environmentally determined, and genotypes may differ in their propensity to develop into gynes or workers under a given set of environmental conditions (4, 8). Historically, genetic variation among individuals has not been thought to contribute to caste determination, although a number of scattered publications have suggested a role for genetic differences, especially in the ants (9-13).However, several recent studies have reported genetic determination of caste in ants. Reproductive females in some species of ants are produced clonally, whereas workers are produced sexually [e.g., Cataglyphis cursor (14); Wasmannia auropunctata (15)]. Some populations of harvester ants (Pogonomyrmex) comprise two independent but interacting genetic lineages. The genome of reproductive females in such populations is composed of a single lineage, whereas females that contain genes from both lineages become workers (16)(17)(18). A similar phenomenon occurs in hybridizing populations of fire ant species (19). In these species, there is a clear genetic effect.A second set of studies involves species with polyandrous queens that find differences in the distribution of male genotypes between gyn...

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Determinants of intracolonial relatedness inPogonomyrmex rugosus(Hymenoptera; Formicidae): mating frequency and brood raids

Cited by 56 publications

References 37 publications

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

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

Fine-scale genetic structure and dispersal distance in the harvester ant Pogonomyrmex barbatus

Patriline shifting leads to apparent genetic caste determination in harvester ants

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