Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants (original) (raw)

Genetic polymorphism in leaf-cutting ants is phenotypically plastic

Proceedings of the Royal Society B: Biological Sciences, 2007

Advanced societies owe their success to an efficient division of labour that, in some social insects, is based on specialized worker phenotypes. The system of caste determination in such species is therefore critical. Here, we examine in a leaf-cutting ant ( Acromyrmex echinatior) how a recently discovered genetic influence on caste determination interacts with the social environment. By removing most of one phenotype (large workers; LW) from test colonies, we increased the stimulus for larvae to develop into this caste, while for control colonies we removed a representative sample of all workers so that the stimulus was unchanged. We established the relative tendencies of genotypes to develop into LW by genotyping workers before and after the manipulation. In the control colonies, genotypes were similarly represented in the large worker caste before and after worker removal. In the test colonies, however, this relationship was significantly weaker, demonstrating that the change in environmental stimuli had altered the caste propensity of at least some genotypes. The results indicate that the genetic influence on worker caste determination acts via genotypes differing in their response thresholds to environmental cues and can be conceptualized as a set of overlapping reaction norms. A plastic genetic influence on division of labour has thus evolved convergently in two distantly related polyandrous taxa, the leaf-cutting ants and the honeybees, suggesting that it may be a common, potentially adaptive, property of complex, genetically diverse societies.

Genetic components to caste allocation in a multiple-queen ant species

2011

Reproductive division of labor and the coexistence of distinct castes are hallmarks of insect societies. In social insect species with multiple queens per colony, the fitness of nestmate queens directly depends on the process of caste allocation (i.e., the relative investment in queen, sterile worker and male production). The aim of this study is to investigate the genetic components to the process of caste allocation in a multiple-queen ant species. We conducted controlled crosses in the Argentine ant Linepithema humile and established single-queen colonies to identify maternal and paternal family effects on the relative production of new queens, workers, and males. There were significant effects of parental genetic backgrounds on various aspects of caste allocation: the paternal lineage affected the proportion of queens and workers produced whereas the proportions of queens and males, and females and males were influenced by the interaction between parental lineages. In addition to revealing nonadditive genetic effects on female caste determination in a multiple-queen ant species, this study reveals strong genetic compatibility effects between parental genomes on caste allocation components. K E Y W O R D S : Caste determination, Linepithema humile, Queen specialization, sex ratio, social insects.

Loss of phenotypic plasticity generates genotype-caste association in harvester ants

2004

However, nothing is known about the factors producing such correlations because developmental flexibility of the two genotypes under different conditions has not been investigated experimentally. To address this, we first assessed whether genotype-caste associations are University of Lausanne CH-1015 Lausanne a characteristic feature of colonies throughout the life cycle. We genotyped the first workers produced by Switzerland 2 Department of Neurobiology newly mated queens, who are limited to raising workers because their fat and muscle reserves used to nourish University of Arizona Tucson, AZ 85721 the brood cannot provide enough resources for reproductive offspring [13, 14]. Queens were collected in cop-3 Department of Evolution, Ecology, and Organismal Biology ula along with a male mate, although they had probably previously mated with one or more additional males at The Ohio State University Columbus, OH 43210 the time of collection. Both same-lineage and interlineage matings were collected from the mating swarms (H swarm: 47 same-lineage pairs, 30 interlineage pairs; J swarm: 44 same-lineage pairs, 44 interlineage pairs).

Testing the genetic determination of the soldier caste in the silver ant

Insectes Sociaux, 2015

Division of labor among workers is a hallmark of social insects that has largely contributed to their ecological success. In a number of species, ants in particular, environmental cues have long been recognized to determine the different phenotypes of workers. Recently, however, a genetic basis for worker polymorphism has been documented in some species. The silver ant Cataglyphis bombycina is characterized by the coexistence of two physiologically distinct castes of non-reproductive individuals: workers and soldiers. Soldiers are not a worker subcaste; they belong to a third caste, along with the queen and the worker castes. Using microsatellite DNA markers, we tested whether soldier caste determination has a genetic component, by comparing the distribution of patrilines between the soldier and the worker castes. Our data show evidence of genotypic variation in caste propensity in only 2 out of 7 colonies sampled. In addition, most patrilines produce both workers and soldiers across all colonies. These results support moderate genotypic influence to soldier caste determination and suggest that non-genetic, likely environmental factors, also influence caste fate among nonreproductive offspring in this species. We also provide new estimates of the queen mating frequency, which support biogeographic variations in mating behavior in C. bombycina.

Phenotypic plasticity in an ant with strong caste–genotype association

Biology Letters, 2018

Caste determination in social Hymenoptera (whether a female egg develops into a reproductive queen or a sterile worker) is a remarkable example of phenotypic plasticity where females with highly similar genomes exhibit striking differences in morphology and behaviour. This phenotypic dichotomy is typically influenced by environmental factors. However, recent studies have revealed a strong caste-genotype association in hybridogenetic ants: workers are all interlineage hybrids while queens are all purebred, suggesting that female caste fate is genetically determined. Using the hybridogenetic ant Cataglyphis mauritanica, we show that under laboratory conditions, purebred offspring develop into reproductive queens but occasionally give rise to workers. Moreover, while hybrids typically become workers, juvenile hormone treatment can switch their developmental pathway to the reproductive caste. These results indicate that phenotypic plasticity has been retained in an ant with a strong caste-genotype association, despite its lack of expression in natural conditions.

Proximate mechanisms and evolution of caste polyphenism in social insects: From sociality to genes

Ecological Research, 2004

Evidence has accumulated over several decades to prove the kin selection theory of evolution of social insects, however, proximate mechanisms of social behavior, and/or caste differentiation remain obscure. Genes that regulate these mechanisms are apparently selected through kin selection, and organisms have consequently acquired sociality. Here, I will discuss several studies that were performed recently by Matsumoto Laboratory, University of Tokyo, Tokyo, Japan, in various social insects, such as termites and ants, in order to reveal the regulatory mechanisms of social behavior and the evolutionary processes of sociality. First, I will review the foraging behavior of the black marching termite Hospitalitermes medioflavus, where well-organized task allocation among castes is apparent. This suggests that regulation of postembryonic development is important in social behavior. Next, I will summarize recent progress in identifying caste-specific gene expression in the damp-wood termite Hodotermopsis sjostedti. This constitutes the basis for molecular mechanisms of caste differentiation, and moreover, the genes identified might be good markers for social evolution. Finally, the mechanism underlying winglessness in ant workers is reviewed. Apoptotic cell death was detected at the stage of pupation in wingless worker castes. Furthermore, the areas of study recently designated as 'sociogenomics' and 'ecological developmental biology' are discussed.

Geographic variation in caste structure among ant populations

Morphologically distinct worker castes of eusocial insects specialize in different tasks. The relative proportions of these castes and their body sizes represent the demography of a colony that is predicted to vary adaptively with environments. Despite strong theoretical foundations, there has been little empirical evidence for the evolution of colony demography in nature. We show that geographically distinct populations of the ant Pheidole morrisi differ in worker caste ratios and worker body sizes in a manner consistent with microevolutionary divergence. We further show that the developmental mechanism for caste determination accounts for the unique pattern of covariation observed in these two traits. Behavioral data reveal that the frequency of different tasks performed by workers changes in a caste-specific manner when caste ratios are altered and demonstrate the importance of the major caste in colony defense. The population-level variation documented here for P. morrisi colonies supports the predictions of adaptive demography theory and illustrates that developmental mechanisms can play a significant role in shaping the evolution of phenotype at the colony level.

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

Behavioral Ecology and Sociobiology, 2005

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 (h 2 =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 multiplequeen 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 broodtenders, 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.

The evolution of caste polymorphism in social insects:0 Genetic release followed by diversifying evolution

Journal of Genetics, 1997

Caste polymorphism, defined as the presence within a colony of two or more morphologically differentiated individuals of the same sex, is an important character of highly eusocial insects both in the Hymenoptera (ants, bees and wasps) and in the Isoptera (termites), the only two groups in the animal kingdom where highly eusocial species occur. Frequently, caste polymorphism extends beyond mere variations in size (although the extent of variations in size can be in the extreme) and is accompanied by allometric variations in certain body parts. How such polymorphism has evolved and why, in its extreme form, it is essentially restricted to the social insects are questions of obvious interest but without satisfactory answers at the present time. I present a hypothesis entitled 'genetic release followed by diversifying evolution', that provides potential answers to these questions. I argue that genetic release followed by diversifying evolution is made possible under a number of circumstances. One of them I propose is when some individuals in a species begin to rely on the indirect component of inclusive fitness while others continue to rely largely on the direct component, as workers and queens in social insects are expected to do. Thus when queens begin to rely on workers for most of the foraging, nest building and brood care, and workers begin to rely increasingly on queens to lay eggs-when queen traits and worker traits do not have to be expressed in the same individual-1 postulate the relaxation of stabilizing selection and new spurts of directional selection on both queen-trait genes and worker-trait genes (in contrasting directions) leading to caste polymorphism.