Division of labour within and between the worker and queen castes is thought to underlie the tremendous success of social insects. Colonies might benefit if subsets of nurse workers specialize ...further in caring for larvae of a certain stage or caste, given that larval nutritional requirements depend on stage and caste. We used short-term (<1 h) and long-term (10 days) behavioural observations to determine whether nurses of the pharaoh ant, Monomorium pharaonis, exhibit such specialization. We found evidence for behavioural specialization among nurses based on larval instar but not larval caste. This specialization was widespread, with 56% of nurses in the short-term and 22–27% in the long-term showing significant specialization. Additionally, we identified ∼200 genes that were differentially expressed in nurse head and abdominal tissues between nurses feeding young versus old larvae. These included 18 genes predicted to code for secreted proteins, which may be passed from nurses to larvae via trophallaxis, as well as vitellogenin and major royal jelly protein-1, which have previously been implicated in the transfer of nutrition from nurse to larvae and the regulation of larval development and caste in social insects. Altogether, our results provide the first evidence in any social insect for a division of labour among nurse workers based on larval stage, and our study begins to elucidate the molecular mechanisms underlying this specialization.
•Ant nurse workers behaviourally specialize on caring for young or old larvae.•Specialists are especially active, performing more feedings than nonspecialists.•Nurse transcriptomic profiles differ between nurses feeding young and old larvae.•Differentially expressed genes include vitellogenin and major royal jelly protein-1.
In insect societies, worker vs. queen development (reproductive caste) is typically governed by environmental factors, but many Pogonomyrmex seed‐harvester ants exhibit strict genetic caste ...determination, resulting in an obligate mutualism between two reproductively isolated lineages. Same‐lineage matings produce fertile queens while alternate‐lineage matings produce sterile workers. Because new virgin queens mate randomly with multiple males of each lineage type, and both worker and queen phenotypes are required for colony growth and future reproduction, fitness is influenced by the relative frequency of each lineage involved in the mutualistic breeding system. While models based solely on frequency‐dependent selection predict the convergence of lineage frequencies towards equal (0.5/0.5), we surveyed the lineage ratios of 49 systems across the range of the mutualism and found that the global lineage frequency differed significantly from equal. Multiple regression analysis of our system survey data revealed that the density and relative frequency of one lineage decreases at lower elevations, while the frequency of the alternate lineage increases with total colony density. While the production of the first worker cohort is largely frequency dependent, relying on the random acquisition of worker‐biased sperm stores, subsequent colony growth is independent of lineage frequency. We provide a simulation model showing that a net ecological advantage held by one lineage can lead to the maintenance of stable but asymmetric lineage frequencies. Collectively, these findings suggest that a combination of frequency‐dependent and frequency‐independent mechanisms can generate many different localized and independently evolving system equilibria.
1. Multiple mating by queens has been shown to enhance disease resistance in insect societies, because higher genetic diversity among nestmates improves collective immune defences or offers a certain ...level of herd immunity. However, it has remained ambiguous whether polygynous societies with large numbers of queens also benefit from increased genetic diversity.
2. We used one of the very few ant species that can be reared across generations, the pharaoh ant, Monomorium pharaonis Linnaeus, to create experimental colonies with two types of enhanced genetic diversity: (i) mixed workers from three divergent inbred lineages representing the ‘polygyny‐equivalent' of multiple mating by queens (i.e. increased between‐worker variation); and (ii) uniform workers whose overall heterozygosity was increased by two subsequent generations of crossing between the same divergent inbred lineages (i.e. increased within‐worker variation).
3. We found significant differences in worker survival among the three inbred lineages, with exposure to conidiospores of the fungal pathogen Beauveria bassiana causing significant mortality to the workers independently of their diversity type. Increased diversity did not improve the resistance to Beauveria.
4. Enhanced heterozygosity colonies had worker survival rates similar to the most resistant inbred lineage, whereas colonies with mixed workers from the three inbred lineages had lower worker and larval survival. Workers did not show any infection‐avoidance behaviour.
5. Average larval survival appeared unaffected by the presence of conidiospores. It benefitted from increased heterozygosity but was reduced in mixed colonies independent of infection. This suggests that negative, but cryptic social interactions in mixed colonies may affect overall survival.
6. The present results do not provide evidence for or against a link between increased genetic variation and increased disease resistance in pharaoh ants, but show that colonies differ considerably in general survival. Thus, increasing the genetic diversity of pharaoh ant colonies may not provide survival advantages in the face of pathogen exposure, and polygyny and polyandry may not be directly comparable mechanisms for creating adaptive resistance towards pathogens.
While reproductive caste in eusocial insects is usually determined by environmental factors, in some populations of the harvester ants, Pogonomyrmex barbatus and P. rugosus, caste has been shown to ...have a strong genetic component. This system of genetic caste determination (GCD) is characterized by between-caste nuclear variation and high levels of mitochondrial haplotype variation between alternative maternal lineages. Two previous genetic models, involving a single nuclear caste-determining locus or interactions between two nuclear loci, respectively, have been proposed to explain the GCD system. We propose a new model based on interactions between nuclear and mitochondrial genes that can better explain the co-maintenance of distinct nuclear and mitochondrial lineages. In our model, females with coevolved cyto-nuclear gene complexes, derived from intra-lineage mating, develop into gynes, while females with disrupted cyto-nuclear complexes, derived from inter-lineage mating, develop into workers. Both haplodiploidy and inbreeding facilitate the buildup of such coevolved cyto-nuclear complexes within lineages. In addition, the opportunity for both intra-lineage and inter-lineage mating in polyandrous populations facilitates the accumulation of gyne-biasing genes. This model may also help to explain the evolution of workerless social parasites. We discuss similarities of GCD and cytoplasmic male sterility in plants and how worker production of males would affect the stability of GCD. Finally, we propose experiments and observations that might help resolve the origin and maintenance of this unusual system of caste determination.
Arising from: G. Wild, A. Gardner & S. A. West Nature 459, 983-986 (2009); Wild, Gardner & West replyWild et al. argue that the evolution of reduced virulence can be understood from the perspective ...of inclusive fitness, obviating the need to evoke group selection as a contributing causal factor. Although they acknowledge the mathematical equivalence of the inclusive fitness and multilevel selection approaches, they conclude that reduced virulence can be viewed entirely as an individual-level adaptation by the parasite. Here we show that their model is a well-known special case of the more general theory of multilevel selection, and that the cause of reduced virulence resides in the opposition of two processes: within-group and among-group selection. This distinction is important in light of the current controversy among evolutionary biologists in which some continue to affirm that natural selection centres only and always at the level of the individual organism or gene, despite mathematical demonstrations that evolutionary dynamics must be described by selection at various levels in the hierarchy of biological organization.
When social interactions occur, the phenotype of an individual is influenced directly by its own genes (direct genetic effects) but also indirectly by genes expressed in social partners (indirect ...genetic effects). Social insect colonies are characterized by extensive behavioral interactions among workers, brood, and queens so that indirect genetic effects are particularly relevant. I used a series of experimental manipulations to disentangle the contribution of direct effects, maternal (queen) effects, and sibsocial (worker) effects to variation for worker, gyne, and male mass; caste ratio; and sex ratio in the ant Temnothorax curvispinosus. The results indicate genetic variance for direct, maternal, and sibsocial effects for all traits, except for male mass there was no significant maternal variance, and for sex ratio the variance for direct effects was not separable from maternal variance for the primary sex ratio. Estimates of genetic correlations between direct, maternal, and sibsocial effects were generally negative, indicating that these effects may not evolve independently. These results have broad implications for social insect evolution. For example, the genetic architecture underlying social insect traits may constrain the realization of evolutionary conflicts between social partners.
In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste ...determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.
PDF
