Colony Genetic Diversity Research Articles

Neonicotinoid exposure increases Varroa destructor (Mesostigmata: Varroidae) mite parasitism severity in honey bee colonies and is not mitigated by increased colony genetic diversity.

Agrochemical exposure is a major contributor to ecological declines worldwide, including the loss of crucial pollinator species. In addition to direct toxicity, field-relevant doses of pesticides can increase species' vulnerabilities to other stressors, including parasites. Experimental field demonstrations of potential interactive effects of pesticides and additional stressors are rare, as are tests of mechanisms via which pollinators tolerate pesticides. Here, we controlled honey bee colony exposure to field-relevant concentrations of 2 neonicotinoid insecticides (clothianidin and thiamethoxam) in pollen and simultaneously manipulated intracolony genetic heterogeneity. We showed that exposure increased rates of Varroa destructor (Anderson and Trueman) parasitism and that while increased genetic heterogeneity overall improved survivability, it did not reduce the negative effect size of neonicotinoid exposure. This study is, to our knowledge, the first experimental field demonstration of how neonicotinoid exposure can increase V. destructor populations in honey bees and also demonstrates that colony genetic diversity cannot mitigate the effects of neonicotinoid pesticides.

Are There Edge Effects on the Genetic Diversity of the Trap-Jaw Ant Odontomachus chelifer (Formicidae: Ponerinae) in a Neotropical Savanna Fragment? A First Assessment.

Habitat fragmentation is considered an important threat to biodiversity, increasing species exposure to edge effects. The Brazilian Cerrado savanna is considered a biodiversity hotspot and has been converted to small, isolated fragments due to human activities. Ant communities and colony survivorship are known to be affected by edge effects in Cerrado, but to date there is no information on the genetic diversity of ant colonies at the edge of fragmented areas. Here, we investigate if colony genetic diversity and structure of Odontomachus chelifer (Latreille) ants (Hymenoptera: Formicidae) are subject to edge effects in a Cerrado reserve in southeast Brazil. Using microsatellites, we evaluated the number of breeders (queens and males) and the genetic diversity in O. chelifer colonies located in the interior versus edge of a Cerrado fragment. All O. chelifer nests had multiple queens, which presented a low mating frequency. The number of breeders and most estimates of genetic diversity did not differ between colonies at the edge versus interior of the fragment. Genetic structure was not influenced by nest location as well. However, we detected a small and positive increase in the observed heterozygosity in colonies located at fragment edges. High heterozygosity is thought to be particularly important in fast-changing environments, such as edges, providing an advantage for genetic diversity. Further investigation is needed to assess in greater detail how habitat loss affects O. chelifer biology. Our study is a first step toward elucidating edge effects on genetic diversity of ant colonies, a topic still poorly explored in tropical environments.

Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants. Acromyrmex leaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South American Acromyrmex species to study how different selective pressures influence the evolution of polygyny and polyandry. We show that Acromyrmex species exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species, Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species, A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution in Acromyrmex leaf-cutting ants.Significance statementMany species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

Estimation of C-derived introgression into A. m. mellifera colonies in the Russian Urals using microsatellite genotyping.

Marker-assisted selection is well established in animal breeding method of selecting individuals with desirable traits in a breeding scheme based on DNA molecular marker patterns. Genetic diversity and C-derived admixture into local purebred gene pool of A. m. mellifera colonies was assessed using polymorphism of nine microsatellite loci in order to provide further marker-assisted selection of desired honey bee colonies. The genetic diversity and the level of C-derived introgression into A. m. mellifera colonies in the Shulgan-Tash Nature Reserve (Russia) was assessed based on nine microsatellite loci (ap243, 4a110, A24, A8, A43, A113, A88, Ap049, A28), which were analized using the fragment analysis of the PCR products in Applied Biosystems 3130 DNA Analyzer. Phylogenetic relationship of colonies was evaluated using Neighbor-Joining methods with Cavalli-Sforza and Edwards genetic distance using the PHYLIP 3.68. The model-based Bayesian clustering algorithm implemented in STRUCTURE2.3.3 was employed to infer membership and introgression proportions (Q-value). In the Shulgan-Tash Nature Reserve colonies of A. m. mellifera subdivided into four groups by level of C-derived introgression. Only five colonies of A. m. mellifera had C-derived introgression which varied from 0.5 to 2%. The genetic diversity in colonies of A. m. mellifera varied from 0.12 to 0.40. The Neighbor-Joining tree demonstrates the genetic relationship of A. m. mellifera colonies, which subdivided into three groups with different levels of C-derived introgression. Group 1 combined five honey bee colonies Bort_1, Bort_2, Bort_3, Baisalyan_1, and Kush_7 with a fraction of introgression close to 0.000 and genetic diversity from 0.20 to 0.25. The results showed the excellence of nine microsatellite loci genotyping in estimation of genetic diversity, distinguishing the two European evolutionary lineages M and C and estimating C-derived introgression. These genetic parameters can be applied further to perform the marker-assisted selection of purebred dark European honey bees.

Physical interactions reduce the power of natural selection in growing yeast colonies

Microbial populations often assemble in dense populations in which proliferating individuals exert mechanical forces on the nearby cells. Here, we use yeast strains whose doubling times depend differently on temperature to show that physical interactions among cells affect the competition between different genotypes in growing yeast colonies. Our experiments demonstrate that these physical interactions have two related effects: they cause the prolonged survival of slower-growing strains at the actively-growing frontier of the colony and cause faster-growing strains to increase their frequency more slowly than expected in the absence of physical interactions. These effects also promote the survival of slower-growing strains and the maintenance of genetic diversity in colonies grown in time-varying environments. A continuum model inspired by overdamped hydrodynamics reproduces the experiments and predicts that the strength of natural selection depends on the width of the actively growing layer at the colony frontier. We verify these predictions experimentally. The reduced power of natural selection observed here may favor the maintenance of drug-resistant cells in microbial populations and could explain the apparent neutrality of interclone competition within tumors.

Neonicotinoid pesticides can reduce honeybee colony genetic diversity.

Neonicotinoid insecticides can cause a variety of adverse sub-lethal effects in bees. In social species such as the honeybee, Apis mellifera, queens are essential for reproduction and colony functioning. Therefore, any negative effect of these agricultural chemicals on the mating success of queens may have serious consequences for the fitness of the entire colony. Queens were exposed to the common neonicotinoid pesticides thiamethoxam and clothianidin during their developmental stage. After mating, their spermathecae were dissected to count the number of stored spermatozoa. Furthermore, their worker offspring were genotyped with DNA microsatellites to determine the number of matings and the genotypic composition of the colony. Colonies providing the male mating partners were also inferred. Both neonicotinoid and control queens mated with drones originating from the same drone source colonies, and stored similar number of spermatozoa. However, queens reared in colonies exposed to both neonicotinoids experienced fewer matings. This resulted in a reduction of the genetic diversity in their colonies (i.e. higher intracolonial relatedness). As decreased genetic diversity among worker bees is known to negatively affect colony vitality, neonicotinoids may have a cryptic effect on colony health by reducing the mating frequency of queens.

Evolution of reproductive traits in Cataglyphis desert ants: mating frequency, queen number, and thelytoky

Cataglyphis desert ants display unique variation in their breeding systems, making this genus a particularly interesting model to study the evolution of derived reproductive traits in eusocial Hymenoptera. Colonies may be headed by a single or several queens, and queens may be singly or multiply mated. Furthermore, in a number of species, both the workers and queens do reproduce asexually by thelytokous parthenogenesis. We examined whether the variability in reproductive traits is the result of a single evolutionary transition or of multiple independent evolutionary transitions, per trait. First, we inferred a phylogenetic estimate for the genus by analyzing DNA sequence variation among several species at four independent loci. Our phylogenetic hypothesis confirms the monophyly of previously defined species groups. Second, we examined the evolution of four reproductive traits in the genus (queen mating frequency, colony queen number, as well as worker reproduction and queen reproduction by thelytokous parthenogenesis), by inferring the state of these traits at the ancestral nodes. Our results show that polyandry and monogyny are the most likely conditions for the ancestor of the genus; the status of worker and queen thelytoky remains ambiguous. Genetic diversity within colonies may have been a major driver for the evolution of derived reproductive traits in Cataglyphis. Kinship among group members has long been recognized as a main factor promoting the evolution of sociality and reproductive altruism. In eusocial Hymenoptera (ants, bees, wasps), at least three reproductive characteristics were shown to profoundly affect colony kin structure and may have played a key role in the evolution and maintenance of reproductive altruism: the queen mating frequency, the number of reproductive queens in a colony, and reproduction by parthenogenesis. We infer the evolution of these three reproductive traits in Cataglyphis desert ants, a genus displaying considerable variation in reproductive strategies. We propose a phylogenetic estimate for the genus, from variation at four loci. Then, we show that multiple evolutionary changes occurred for all three reproductive characters studied. Our results suggest that selection for enhanced colony genetic diversity has driven the evolution of reproductive traits away from their ancestral state.

Population genetics of the California National Primate Research Center's (CNPRC) captive Callicebus cupreus colony.

The California National Primate Research Center maintains a small colony of titi monkeys (Callicebus cupreus) for behavioral studies. While short tandem repeat (STR) markers are critical for the genetic management of the center's rhesus macaque (Macaca mulatta) breeding colony, STRs are not used for this purpose in the maintenance of the center's titi monkey colony. Consequently, the genetic structure of this titi monkey population has not been characterized. A lack of highly informative genetic markers in titi monkeys has also resulted in scant knowledge of the species' genetic variation in the wild. The purpose of this study was to develop a panel of highly polymorphic titi monkey STRs using a cross-species polymerase chain reaction (PCR) amplification protocol that could be used for the genetic management of the titi monkey colony. We screened 16 STR primer pairs and selected those that generated robust and reproducible polymorphic amplicons. Loci that were found to be highly polymorphic, very likely to be useful for parentage verification, pedigree assessment, and studying titi monkey population genetics, were validated using Hardy-Weinberg equilibrium and linkage disequilibrium analyses. The genetic data generated in this study were also used to assess directly the impact on the colony's genetic diversity of a recent adenovirus outbreak. While the adenovirus epizootic disease caused significant mortality (19 deaths among the 65 colony animals), our results suggest that the disease exhibited little or no influence on the overall genetic diversity of the colony.

Colony genetic diversity affects task performance in the red ant Myrmica rubra

High relatedness and low genetic diversity among individuals in a group is generally considered crucial to the evolution of cooperative behaviour. However, in about a third of social insect species, intracolonial genetic diversity is increased because of derived polyandry (multiple mating by queens) and/or polygyny (multiple reproductive queens). Several studies have shown that increased intracolonial genetic diversity can enhance task performance in honey bees, but evidence of such effect in other social insects is still lacking. Why increased genetic diversity has evolved in some, but not all species, is a fundamental question in sociobiology. In this study, we investigated the effect of intracolonial genetic diversity on the task of nest migration, using the facultatively polyandrous and polygynous red ant Myrmica rubra. Genetic diversity significantly affected migration speed, but its effects were context dependent. Migration speed correlated positively with genetic diversity in one experiment in which migrations were into a known nest site, due to quicker transfer of brood into the new nest once consensus was reached. However, in a another experiment in which migration included scouting for new nest sites, migration speed correlated negatively with genetic diversity, due to slower discovery of new nest sites and slower transfer of brood into the new nest. Our results show for the first time that genetic diversity affects task performance in a social insect other than the honeybee, but that it can produce contrasting effects under different conditions.

Multiple Mating But Not Recombination Causes Quantitative Increase in Offspring Genetic Diversity for Varying Genetic Architectures

Explaining the evolution of sex and recombination is particularly intriguing for some species of eusocial insects because they display exceptionally high mating frequencies and genomic recombination rates. Explanations for both phenomena are based on the notion that both increase colony genetic diversity, with demonstrated benefits for colony disease resistance and division of labor. However, the relative contributions of mating number and recombination rate to colony genetic diversity have never been simultaneously assessed. Our study simulates colonies, assuming different mating numbers, recombination rates, and genetic architectures, to assess their worker genotypic diversity. The number of loci has a strong negative effect on genotypic diversity when the allelic effects are inversely scaled to locus number. In contrast, dominance, epistasis, lethal effects, or limiting the allelic diversity at each locus does not significantly affect the model outcomes. Mating number increases colony genotypic variance and lowers variation among colonies with quickly diminishing returns. Genomic recombination rate does not affect intra- and inter-colonial genotypic variance, regardless of mating frequency and genetic architecture. Recombination slightly increases the genotypic range of colonies and more strongly the number of workers with unique allele combinations across all loci. Overall, our study contradicts the argument that the exceptionally high recombination rates cause a quantitative increase in offspring genotypic diversity across one generation. Alternative explanations for the evolution of high recombination rates in social insects are therefore needed. Short-term benefits are central to most explanations of the evolution of multiple mating and high recombination rates in social insects but our results also apply to other species.

Experimental Conversion of Colony Social Organization in Fire Ants (Solenopsis invicta): Worker Genotype Manipulation in the Absence of Queen Effects

Colony social organization in the fire ant Solenopsis invicta appears to be under strong genetic control. In the invasive USA range, polygyny (multiple queens per colony) is marked by the presence of the Gp-9b allele in most of a colony’s workers, whereas monogyny (single queen per colony) is associated with the exclusive occurrence of the Gp-9B allele. Ross and Keller, Behav Ecol Sociobiol 51:287–295 (2002) experimentally manipulated social organization by cross-fostering queens into colonies of the alternate form, thereby changing adult worker Gp-9 genotype frequencies over time. Although these authors showed that social behavior switched predictably when the frequency of b-bearing adult workers crossed a threshold of 5–10%, the possibility that queen effects caused the conversions could not be excluded entirely. We addressed this problem by fostering polygyne brood into queenright monogyne colonies. All such treatment colonies switched social organization to become polygyne, coincident with their proportions of b-bearing workers exceeding 12%. Our results support the conclusion that polygyny in S. invicta is induced by a minimum frequency of colony workers carrying the b allele, and further confirm that its expression is independent of queen genotype or history, worker genotypes at genes not linked to Gp-9, and colony genetic diversity.

Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors

Division of labour among workers is central to the organisation and ecological success of insect societies. If there is a genetic component to worker size, morphology or task preference, an increase in colony genetic diversity arising from the presence of multiple breeders per colony might improve division of labour. We studied the genetic basis of worker size and task preference in Formica selysi, an ant species that shows natural variation in the number of mates per queen and the number of queens per colony. Worker size had a heritable component in colonies headed by a doubly mated queen (h2=0.26) and differed significantly among matrilines in multiple-queen colonies. However, higher levels of genetic diversity did not result in more polymorphic workers across single- or multiple-queen colonies. In addition, workers from multiple-queen colonies were consistently smaller and less polymorphic than workers from single-queen colonies. The relationship between task, body size and genetic lineage appeared to be complex. Foragers were significantly larger than brood-tenders, which may provide energetic or ergonomic advantages to the colony. Task specialisation was also often associated with genetic lineage. However, genetic lineage and body size were often correlated with task independently of each other, suggesting that the allocation of workers to tasks is modulated by multiple factors. Overall, these results indicate that an increase in colony genetic diversity does not increase worker size polymorphism but might improve colony homeostasis.

Experimental manipulation of colony genetic diversity had no effect on short-term task efficiency in the Argentine ant Linepithema humile

Genetic diversity might increase the performance of social groups by improving task efficiency or disease resistance, but direct experimental tests of these hypotheses are rare. We manipulated the level of genetic diversity in colonies of the Argentine ant Linepithema humile, and then recorded the short-term task efficiency of these experimental colonies. The efficiency of low and high genetic diversity colonies did not differ significantly for any of the following tasks: exploring a new territory, foraging, moving to a new nest site, or removing corpses. The tests were powerful enough to detect large effects, but may have failed to detect small differences. Indeed, observed effect sizes were generally small, except for the time to create a trail during nest emigration. In addition, genetic diversity had no statistically significant impact on the number of workers, males and females produced by the colony, but these tests had low power. Higher genetic diversity also did not result in lower variance in task efficiency and productivity. In contrast to genetic diversity, colony size was positively correlated with the efficiency at performing most tasks and with colony productivity. Altogether, these results suggest that genetic diversity does not strongly improve short-term task efficiency in L. humile, but that worker number is a key factor determining the success of this invasive species.

Paternity in eusocial Hymenoptera

Variation in paternity frequency in colonies of eusocial insects has profound effects on the relatedness among offspring and on the genetic diversity of colonies. Data on queen ‘mating-frequency’ in eusocial Hymenoptera vary in both quality and the phase of the ‘mating’ process they address. Some are observational studies of the range or maximum number of copulations; others are derived from estimates of the number of sperm in males and queens; others use genetic techniques to determine the paternity of different males among female offspring. Only the latter data can be used to calculate relatedness among offspring females. Previous reviews drew attention to these problems, but their results have established the impression that high paternity frequencies are common, largely because multiple copulations are frequently observed. For ants, we show that: (i) the range of observed copulations overestimates effective paternity frequency; and (ii) the mean effective paternity frequency in 19 species, for which accurate data based on allozyme analysis of mother — offspring combinations are available, is only 1.16 (range 1-1.48). Over one third of these species have queens in which only one male contributes to paternity. Data from 34 species, which include less detailed genetic studies and four species studied using sperm counts, give similar results. Only two species, bothAttaleaf cutter ants and both studied using data on sperm stored in queen spermathecas, appear to have effective insemination frequencies above two. Data on bees and wasps show a similar trend. We conclude that reliably documented high paternity or insemination frequencies (> 2) are currently restricted to one phylogenetically isolated and highly eusocial taxon each in ants, eusocial bees and wasps (Atta, ApisandVespula, respectively). This pattern justifies the working hypothesis that multiple mating, by lowering the relatedness between female offspring and thereby the benefits of reproductive helping behaviour, has not been a general constraint for the evolution of eusociality in the Hymenoptera. Using reliable data on paternity frequency and insemination, we re-analyse two factors that it has been suggested correlate with mating frequency: colony population and number of egg-laying queens per colony. We find the following. 1. There is a significant positive correlation between paternity/insemination frequency and colony size for monogynous ants, but not for polygynous ants. This result seems to support the ‘sperm limitation’ hypothesis, that queens which need to be highly fecund copulate multiply to store sufficient sperm. We note, however, that the same trend is expected when large and/or long-lived colonies profit more from having genetically diverse offspring. 2. There is no significant negative correlation between paternity/insemination frequency and number of queens per colony. However, when the analysis is restricted to species with large colonies and no intranidal mating, the correlation between paternity frequency and queen number becomes marginally significant. Several previous reviews have addressed the possible adaptive significance of multiple paternity. In contrast, and in keeping with the data that show single paternity to be frequent, we discuss selective reasons for single or low paternity. We compare the relative effects of multiple paternity and multiple maternity on genetic diversity within colonies and show that they are not equivalent, and we also discuss directions for future research on paternity issues in social insects.