The neural and hormonal basis of the loss of parental care in threespine stickleback

Maciejewski, Meghan F.

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https://hdl.handle.net/2142/129921 Copy

Description

Title

The neural and hormonal basis of the loss of parental care in threespine stickleback

Author(s)

Maciejewski, Meghan F.

Issue Date

2025-07-08

Director of Research (if dissertation) or Advisor (if thesis)

Bell, Alison M

Doctoral Committee Chair(s)

Bell, Alison M

Committee Member(s)

• Fuller, Becky C
• Fischer, Eva K
• Hauber, Mark E

Department of Study

Evolution Ecology Behavior

Discipline

Biology

Degree Granting Institution

University of Illinois Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• stickleback
• parental care
• neuropeptide
• oxytocin
• steroid

Abstract

Social behaviors show immense diversity across animals, yet they are often regulated by brain regions and molecules (e.g., the preoptic area of the hypothalamus (POA), oxytocin, and testosterone) that are repeatedly recruited and repurposed by selection. How do these conserved mechanisms give rise to such diverse behavioral phenotypes? These neural and hormonal systems can be tweaked in many ways: the number and activity of specific neuronal populations, the activity of brain regions or networks of brain regions, the expression and binding affinity of hormone receptors, levels of hormone ligands, etc. Certain elements of these systems may be more evolutionarily labile than others and, therefore, may be more likely to drive evolutionary divergence in behavior. Here, I investigate the role of conserved “neuroendocrine building blocks” in the behavioral divergence of two recently diverged populations (ecotypes) of threespine stickleback (Gasterosteus aculeatus): “whites” and “commons.” Males of the common ecotype provide obligate uniparental care to their offspring after mating; males of the white ecotype provide no care. Instead, whites “disperse” their embryos soon after fertilization by spitting them out of the nest. This recent evolutionary loss of parental care in whites offers a fascinating opportunity to test how canonical building blocks of parental care - the POA, neuropeptide hormones, and steroid hormones - are tweaked when care is lost. What role do these building blocks play in the initiation and maintenance of fatherhood in commons, and what has been lost in whites? In Chapter 1, I provide an overview of the parental care literature to demonstrate how non-mammalian models, like stickleback, can expand our understanding of paternal care and its evolution (Maciejewski and Bell, 2022). In Chapter 2, I investigate how the number and activity of conserved neuropeptidergic neurons in the POA (oxytocin and galanin), as well as the overall activity of neurons in the POA, change across stages of care and differ between ecotypes (Maciejewski et al., in press). In commons, but not whites, the activity of preoptic oxytocin and galanin neurons changes across stages of care, suggesting that these neurons play an important role in initiating care behavior. A loss of this activation could contribute to the loss of care in whites. In Chapter 3, I delve deeper into the role of oxytocin in the loss of care by pharmacologically manipulating oxytocin levels in whites and commons after mating (Dan and Maciejewski et al., 2024). The results show that perturbation of the oxytocin system affects the initiation of care in commons but does not increase care or decrease dispersal behavior in whites. Both ecotypes behaviorally responded to oxytocin manipulation, but in unique ways, suggesting that oxytocin may act on different “parental circuits” in the two ecotypes. Finally, in Chapter 4, I characterize whole-body steroid levels in whites and commons to determine if the loss of care is associated with changes in steroid signaling across reproductive stages. The results suggest that high androgens and low progestogens may promote mating behavior in whites and commons, and low androgens and high progestogens may facilitate the switch to parenting in commons. I pose several hypotheses for future studies as to how ecotypic differences in the regulation of androgens and progestogens across stages may have arisen, e.g., gonadotropins, steroid receptors, steroidogenic enzymes, etc. These data add to growing evidence that fatherhood, like motherhood, is a period of immense change in behavior, hormones, and the brain. Commons show changes across reproductive stages in the activation of key neurons in the POA, the sensitivity to neuropeptides, and the levels of androgens and progestogens. The loss of care is characterized by a loss of change. Male whites fail to transition into a caregiving mode after mating and show no changes in the activation of neuropeptidergic neurons in the POA or levels of androgens across stages. Overall, this work provides an example of how losses at the phenotypic level can be paralleled by losses at the mechanistic level and how conserved building blocks can be tweaked in the early stages of behavioral divergence.

Graduation Semester

2025-08

Type of Resource

Thesis

Handle URL

https://hdl.handle.net/2142/129921

Copyright and License Information

Copyright 2025 Meghan Maciejewski

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