Alternative reproductive tactics in females: the case of size polymorphism in ant queens

Alternative reproductive tactics are common in males but rather rare in females. In this respect, ants are apparently an interesting exception. Ant queens can either start a new colony on their own or utilize the work force of existing colonies for dependent colony founding. As the success of these different options depends on body reserves of the queens, the finding of two different classes of alate queens in some ant species that differ only in size strongly suggests alternative modes of reproduction. Studies of queen size polymorphism from a number of ant species differ in scope and also in their results. Nevertheless, across taxa evidence exists that small queens found dependently while their larger conspecifics found colonies on their own. However, in most cases it is not clear whether the small queens exploit unrelated colonies (intraspecific “social parasitism”) or return to their natal colonies. In some ant species the queen size polymorphism might constitute an evolutionary transition to either interspecific social parasitism or a mor-phologically more pronounced queen polymorphism linked to dispersal. In others, queen size polymorphism might be a stable phenomenon. Although it is important in this context whether queen size polymorphism is caused by a genetic polymorphism or phenotypic plasticity, so far no conclusive evidence about proximate mechanisms of size determination has been presented. Some considerations are made about the question why female alternative reproductive tactics correlated with morphological adaptations are comparatively widespread in ants

Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.)

Background The reproductive ground plan hypothesis of social evolution suggests that reproductive controls of a solitary ancestor have been co-opted during social evolution, facilitating the division of labor among social insect workers. Despite substantial empirical support, the generality of this hypothesis is not universally accepted. Thus, we investigated the prediction of particular genes with pleiotropic effects on ovarian traits and social behavior in worker honey bees as a stringent test of the reproductive ground plan hypothesis. We complemented these tests with a comprehensive genome scan for additional quantitative trait loci (QTL) to gain a better understanding of the genetic architecture of the ovary size of honey bee workers, a morphological trait that is significant for understanding social insect caste evolution and general insect biology. Results Back-crossing hybrid European x Africanized honey bee queens to the Africanized parent colony generated two study populations with extraordinarily large worker ovaries. Despite the transgressive ovary phenotypes, several previously mapped QTL for social foraging behavior demonstrated ovary size effects, confirming the prediction of pleiotropic genetic effects on reproductive traits and social behavior. One major QTL for ovary size was detected in each backcross, along with several smaller effects and two QTL for ovary asymmetry. One of the main ovary size QTL coincided with a major QTL for ovary activation, explaining 3/4 of the phenotypic variance, although no simple positive correlation between ovary size and activation was observed. Conclusions Our results provide strong support for the reproductive ground plan hypothesis of evolution in study populations that are independent of the genetic stocks that originally led to the formulation of this hypothesis. As predicted, worker ovary size is genetically linked to multiple correlated traits of the complex division of labor in worker honey bees, known as the pollen hoarding syndrome. The genetic architecture of worker ovary size presumably consists of a combination of trait-specific loci and general regulators that affect the whole behavioral syndrome and may even play a role in caste determination. Several promising candidate genes in the QTL intervals await further study to clarify their potential role in social insect evolution and the regulation of insect fertility in general

A female caste specialized for the production of unfertilized eggs in the ant Crematogaster smithi

In colonies of the North American ant Crematogaster smithi “large workers” occur which are morphologically intermediate between winged queens and small workers and appear to be specialized for the production of unfertilized eggs. In queenless colonies these eggs may develop into males, but most of them are eaten in colonies containing a queen. We discuss the possible significance of this new type of female

A new type of exocrine gland and its function in mass recruitment in the ant Cylindromyrmex whymperi (Formicidae: Cerapachinae)

Workers of the ant Cylindromyrmex whymperi display mass trail recruitment. Bioassays show that the trail pheromone originates from a unique gland between abdominal sternites 6 and 7. The gland has a hitherto unknown structural organization. Upon leaving the secretory cell, the duct cell widens to form a sclerotized pear-shaped reservoir chamber, lined with multiple duct cells. Each duct thus forms a miniature reservoir for the secretions of each single secretory cell, a novel structural arrangement in exocrine glands of social Hymenoptera

Finding the Missing Honey Bee Genes: Lessons Learned from a Genome Upgrade

Background: The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes.Results: Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data.Conclusions: Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination

Mitochondrial markers in the ant Leptothorax rugatulus reveal the population genetic consequences of female philopatry at different hierarchical levels

Leptothorax rugatulus, an abundant North American ant, displays a conspicuous queen size polymorphism that is related to alternative reproductive tactics. Large queens participate mainly in mating flights and found new colonies independent of their mother colony. In contrast, small queens do not found new colonies independently, but seek readoption into their natal nest which results in multiple-queen colonies (polygyny). Populations differ strongly in the ratio of small to large queens, the prevalent reproductive tactic and colony social structure, according to ecological parameters such as nest site stability and population density. This study compares the genetic structure of two strongly differing populations within the same mountain range. Data from microsatellites and mitochondrial DNA give no evidence for alien reproductives in polygynous colonies. The incidence of alien workers in colonies (as determined by mitochondrial haplotype) was low and did not differ between monogynous and polygynous colonies. We found significant population viscosity (isolation-by-distance) at the mitochondrial level in only the predominantly polygynous population, which supports the theoretical prediction that female philopatry leads to mtDNA-specific population structure. Nuclear and mitochondrial genetic diversity was similar in both populations. The genetic differentiation between the two investigated populations was moderate at the mitochondrial level, but not significantly different from zero when measured with microsatellites, which corroborates limited dispersal of females (but not males) at a larger scale

Added weights lead to reduced flight behavior and mating success in polyandrous honey bee queens (Apis mellifera)

Honey bee queens are exceptionally promiscuous. Early in life, queens perform one to five nuptial flights, mating with up to 44 drones. Many studies have documented potential benefits of multiple mating. In contrast, potential costs of polyandry and the sensitivity of queens to such costs have largely been ignored because they are difficult to address experimentally. To consider one aspect of mating costs to queens, the difficulty of flight, we compared flight behavior and success among a group of control queens and two experimental groups of queens that carried lead weights of two different sizes. For each queen, we assessed the number and duration of all flights and, after egg-laying commenced, the amount of stored sperm and the number of mates in terms of the offspring’s patrilineal genetic diversity. Added weights quantitatively decreased the number of flights, the mean duration of flights and consequently the total time spent flying. Mating success in terms of sperm quantity and patrilines detected among the queens’ offspring was also negatively impacted by the experimental manipulation. Thus, it can be concluded that the flight effort of honey bee queens during their mating period is adjusted in response to an experimentally increased cost of flying with multiple consequences for their mating success. Our results suggest that queen behavior is flexible and mating costs deserve more attention to explain the extreme polyandry in honey bees

Complex determination of queen body size in the queen size dimorphic ant Leptothorax rugatulus (Formicidae: Hymenoptera)

In order to understand the evolution of natural variability, and polymorphisms in particular, it is essential to study proximate causes. Our study is the first work on ants to determine formally the heritability of quantitative traits in a quantitative genetic framework. We investigated the causes of queen size dimorphism of the ant Leptothorax rugatulus and derive from the results a possible scenario for its evolutionary maintenance. Mother size was highly predictive of daughter size in field colonies. This finding could be repeated under constant laboratory conditions. Data suggested that maternal effects via egg size are not the cause for the transmission of body size. In colonies with coexisting large and small mother queens, daughter size did not correlate with mother size, and in an additional experiment we found a negative effect of queen number on daughter size. The integration of these various results suggests a high transmissibility of body size from generation to generation. However, social (queen) influences also affect daughter size, especially in the case of mixed colonies. This complex determination fits well with an adaptive adjustment of queen size to alternative reproductive strategies