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Evolutionary Link Between Maternal Behavior and Eusociality Is Supported by Wasp Gene Expression

A defining feature of eusociality is the presence of workers that abstain from reproduction and care for their siblings (i.e., workers forage for food and feed the brood). It has been proposed that this behavior evolved from maternal care behavior and that sibling care and maternal care behaviors are regulated by similiar patterns of gene regulation. Toth et al. assessed this proposal by examining gene expression in the primitively eusocial wasp Polistes metricus using 454 Sequencing; 391,157 brain cDNA reads were generated and resulted in hits to 3,017 genes from the honey bee genome. Orthologs of 32 honey bee behaviorally related genes were identified and analyzed. The gene expression in the brain of P. metricus workers was more similar to that of foundresses, which show maternal care, than to that of queens and gynes, which do not. As insulin-related genes were among the differentially regulated genes, Toth et al. suggest that the evolution of eusociality involved major nutritional and reproductive pathways.

Introduction

Individuals of Polistes metricus specialize as either workers or reproductive individuals but the two castes are not as distinct than they are in more advanced eusocial species. Polistes workers and reproductive individuals show caring behavior, but at different time points in the life of a colony. Therefore, Polistes allows the analysis of the molecular basis of maternal and sibling care within one species.

New colonies are formed in the spring by female foundresses that show reproductive and maternal behavior. When the first generation of female brood has been reared and become workers, the foundresses become queens, stop caring for the brood, and focus on reproduction. The workers take over provisioning their siblings by searching for food and feeding them. They exhibit only little or no reproductive behavior. Late in the season gynes are reared. They do not show any reproductive or maternal behavior. After mating, gynes overwinter and become foundresses. Toth et al. hypothesized that the brain gene expression patterns in P. metricus workers and foundresses should be the most similar among the four groups as they both exihibit caring behavior despite their different reproductive status.

As social behavior is complex and polygenic, the analysis of multiple genes in different pathways is necessary to assess the idea that maternal and worker behavior have a common molecular basis. Therefore, the hitherto lacking genomic sequence information of P. metricus was generated using 454 Sequencing.

Materials and Methods

454 Sequencing was used to obtain 45M base pairs (bp) in 391,157 cDNA sequence fragments from the P. metricus brain transcriptome. A map of the honey bee (Apis mellifera) genome combining known transcripts and their relative abundance in bee EST datasets was generated. The P. metricus transcript fragments predicted to code for orthologous proteins to A. mellifera genes were then plotted to this map according to the number of fragments identified for a particular locus. For 39% of all A. mellifera mRNAs a matching P. metricus fragment was found. Toth et al. used the combined dataset to choose the genes for their study. Gene expression patterns in P. metricus did not influence gene selection

32 candidate genes from the P. metricus EST set were selected (Table 1). These genes are orthologs of A. mellifera genes that are known to be associated with worker behavior. 22 of the genes are differentially expressed in the brains of bees engaged in foraging or feeding and are regulated by juvenile hormone, which also causes worker behavior. Five of the genes are differentially expressed in A. mellifera individuals showing provisioning, three of which also play causal roles in the regulation of foraging behavior. Five additional genes are involved in insulin signaling. These five candidate genes were selected because the insulin pathway is involved in A. mellifera caste determination and worker foraging behavior.

Results and Discussion

The gene expression in the brain of individual wasps was firmly associated with naturally occurring differences in behavior. Leave-one-out cross-validation analysis resulted in 68%, 69%, 70%, and 47% correct assignments to the P. metricus foundress, gyne, queen, and worker groups, respectively. The less conservative resubstitution method resulted in 89%, 100%, 100%, and 95% correct assignments. These predictions were significantly better than random assignment (p<0.0001). The set of 32 genes thus shows differential brain regulation across the four wasp groups, enabling exploration of the molecular relationship between maternal and worker behavior.

62% of the 32 genes were differentially regulated depending on reproductive or provisioning behavior (Figure 1). Three out of five insulin-related genes displayed associations with provisioning and/or reproductive behavior. K-means clustering indicated five clusters of genes that are co-expressed (Figure 1). The first cluster comprises eight genes that are co-expressed in foundresses and workers compared with queens and gynes. The second cluster (7 genes) is upregulated in gynes and the third cluster (6 genes) downregulated in queens. Foundresses and workers showed similar expression patterns for these two gene clusters. Linear discriminant analysis and hierarchical clustering by group also demonstrated similar gene expression in the brains of foundresses and workers (data not shown).

The dramatical temporal changes in brain gene expression as females shift from foundress to queen demonstrate heterochronic expression of genes associated with maternal behavior. This plasticity is thought to be necessary for the evolution of worker behavior. These findings also reflect an apparent modularity of reproductive and caring behavior and their regulatory networks. This type of modularity is considered to be important for the evolution of novel traits.

Conclusions

In this study, 454 Sequencing was used to rapidly generate genomic information hitherto not available for the wasp Polistes metricus. The completely sequenced genome of the relatively closely related honey bee was employed as a “hub” in order to use the genomic information obtained for P. metricus to address a specific evolutionary problem. This “hub and spokes” approach might enable genomics to be developed for a broader range of species.

This article was summarized for BIOCHEMICA using the following original publication:

Toth AL et al. (2007) Science 318:441–444

This article was originally published in Biochemica 1/2008, pages 4-5. ©Springer Medizin Verlag 2008