Student Theses and Dissertations
Date of Award
2025
Document Type
Thesis
Degree Name
Doctor of Philosophy (PhD)
Thesis Advisor
Daniel Kronauer
Keywords
indirect genetic effects, caste determination, clonal raider ants, caregiver genotype, ecdysone signaling, larval growth
Abstract
The distinction between nature (genetics) and nurture (environment) is blurry, in part because the environment includes the genes of social partners. This is especially evident for parents and their offspring, where genes expressed in one partner profoundly influence the physiology and behavior of the other. Such indirect genetic effects (IGEs) are mediated through social interactions. Although parental care has evolved in many disparate lineages, in most systems it is challenging to delineate the effects of genetics and environment on the phenotypes of caregivers and offspring. This is because most animals with parental care reproduce sexually, meaning each genotype is represented by a single individual. Moreover, it is often impossible to control the environment that an individual experiences, which is crucial because a single genotype can generate different phenotypes in response to environmental variation (i.e., gene-by-environment interactions). Given these challenges, despite IGEs being ubiquitous, characterizations of how they occur at the molecular level are scarce and incomplete. Most studies have yielded correlations between genes and phenotypic outcomes in social partners, but do not establish causal relationships. Thus, our understanding of the molecular mechanisms underlying IGEs, including those between caregivers and their young, is limited. As a result, it is unknown whether common molecular factors or general rules underlie IGEs across traits and species. The clonal raider ant, Ooceraea biroi, provides a powerful model in which the effects of genetics and environment on social traits can be disentangled. These ants reproduce parthenogenetically and can be maintained in the laboratory under standardized conditions. Colonies can be assembled with different combinations of caregiver and larval genotypes, enabling measurement of IGEs. Therefore, I investigated the effects of caregiver IGEs on larval growth and development by cross-fostering different clonal genotypes of O. biroi. I found that brood phenotypes, including body size, caste morphology, developmental timing, and survival, are shaped by the genotype of their caregivers. I also found that some IGEs are dependent on caregiver age and number, demonstrating that environment modifies how genes in social partners influence phenotype (i.e., IGE-by-environment interactions). In ants, caste identity is strongly correlated with body size, but whether environmental factors can regulate caste traits independently of size, and thus decouple the two, remains controversial. Thus, I tested whether different environmental factors, including caregiver genotype, temperature, and food availability, can modify the allometric relationship between caste trait expression and body size. I found no evidence that the relationship between caste trait expression and body size varied across conditions, indicating limited or no plasticity in the scaling relationship itself. This suggests that body size and other caste traits are developmentally coupled in ants via systemic molecular factors. In contrast, I found that both body size and the scaling relationship varies between genotypes, implying that genetic variation in body size and/or the allometric relationship can influence caste morphology in ants. This also establishes that studying environmental effects, including IGEs, on caste development is fundamentally tied to examining how environment affects body size. My experiments established that caregiver genotype unconditionally influences the final body size of brood. To investigate the molecular basis of this IGE, I conducted RNA-sequencing on larval and adult tissues from a cross-fostering experiment, identifying a modest set of larval genes whose expression is influenced by caregiver genotype. These included neuropeptide genes known to regulate ecdysone synthesis in the prothoracic gland of other insects, including corazonin, prothoracicotropic hormone, pheromone biosynthesis activating neuropeptide, and shadow, which encodes an enzyme in the ecdysone biosynthesis pathway. Using RNA-FISH, I confirmed that cells of the prothoracic gland in larvae express receptors for these neuropeptides. Functional assays then showed that treating larvae with ecdysone or corazonin reduces final body size without affecting developmental duration. These findings support a conserved role for basal ecdysone in regulating larval growth, reveal its importance in caste determination in ants, and show that its levels are modulated by caregiver IGEs. I also discovered that multiple chemosensory protein (CSP) and odorant-binding protein (OBP) genes, canonically associated with olfaction, are differentially expressed in larvae due to caregiver genotype, and their expression in larvae was localized to cells in the fat body that coexpress Desaturase 1 (Desat1 converts saturated fatty acids into unsaturated fatty acids). Also, gene set enrichment analysis shows that processes related to fatty acid catabolism were impacted by caregiver IGEs. This indirectly implicates CSPs and OBPs as relevant to this process, as they are known to bind and carry fatty acids. In support of this, it was found that expression of Obp5 and Csp14 in the larval fat body was activated by starvation. Furthermore, ecdysone and corazonin treatment of larvae had opposing effects on Csp and Obp expression, with ecdysone downregulating these genes. These findings raise the possibility that ecdysone inhibits larval growth by suppressing Csp/Obp expression and lipid catabolism in the fat body. Considering findings in other insects, I hypothesize that the regulation of Csp/Obp expression by ecdysone signaling may be a general phenomenon that applies across tissues and insects. Overall, this work significantly advances our understanding of the molecular basis by which caregiver IGEs influence larval growth, yet many questions remain open.
License and Reuse Information
This work is licensed under a Creative Commons Attribution-NonCommercial-Share Alike 4.0 International License.
Recommended Citation
Piekarski, Patrick Konrad, "Nurture is Nature: The Molecular Basis of Caregiver Genotype Effects on Larval Growth and Caste Development in the Clonal Raider Ant" (2025). Student Theses and Dissertations. 823.
https://digitalcommons.rockefeller.edu/student_theses_and_dissertations/823
Comments
A thesis presented to the faculty of The Rockefeller University in partial fulfillment of the requirements for the degree of Doctor of Philosophy