The neuroendocrine and molecular mechanisms underlying stress-induced maternal effects in the threespine stickleback

Mommer, Brett

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Description

Title

The neuroendocrine and molecular mechanisms underlying stress-induced maternal effects in the threespine stickleback

Author(s)

Mommer, Brett

Issue Date

2013-08-22T16:47:23Z

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

Bell, Alison M.

Doctoral Committee Chair(s)

Bell, Alison M.

Committee Member(s)

• Fuller, Rebecca C.
• Stubbs, Lisa J.
• Whitfield, Charles W.

Department of Study

School of Integrative Biology

Discipline

Biology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• parental effect
• glucocorticoid
• hypothalamus-pituitary-interrenal (HPI) axis
• predators
• maternal programming
• transcriptome

Abstract

Non-genetic maternal effects occur when offspring phenotype is influenced non-genetically by a mother’s phenotype. Exposure of mothers to external stressors, for example, can influence the expression of a wide array of offspring traits essential for survival, including growth, morphology, and behavior. In fact the exposure of mothers to an ecologically relevant stressor such as a non-lethal predator attack can alter the life-long offspring physiological and behavioral response to the same stressor. The transfer of information about the environment from a mother to her offspring, though, likely depends on the nature of her physical and behavioral contact with them, which in turn depends on the life history of the species. Mothers of many mammalian species, for example, care for offspring postnatally in addition to providing pre- and postnatal resources. The fact that stress-induced maternal effects occur in non-mammalian vertebrates, including many oviparous species that do not exhibit maternal care, indicates that the transgenerational transfer of information can occur entirely through the egg. Little is known, however, about the mechanisms by which mothers transmit information about the environment through the egg or how this information, once received by offspring, influences their phenotype non-genetically. For my PhD research I studied maternal effects in threespine sticklebacks (Gasterosteus aculeatus), with the goal to describe a maternal effect on the physiological stress response and the underlying molecular mechanisms by which the non-genetic maternal effects on physiology and behavior occur in sticklebacks. Sticklebacks are an oviparous fish that do not exhibit maternal care. Further, they are a model species in the study of behavior, easily acclimate and reproduce in a lab setting, and now have a fully sequenced genome, making the species an ideal candidate for the study maternal effects using techniques in genetics, physiology, and behavior. Previous studies in sticklebacks have shown that maternal exposure to predation risk increases the amount of cortisol, a stress hormone, in eggs and affects offspring antipredator behavior, learning, and survival in the presence of live predation. The physiological stress response, coordinated by the hypothalamus-pituitary-interrenal (HPI) axis, is the biological link between the recognition of external stressors by the brain and the broad homeostatic changes that occur in the body in response to those stressors. The diversity of offspring behavioral responses to maternal stress in sticklebacks therefore suggests organizational effects on the HPI axis, though to date this has not been tested. Therefore the first chapter of my thesis (Chapter 2) tested the hypothesis that maternal exposure to predation risk has long-lasting effects on the stress response of offspring in sticklebacks. To accomplish this I exposed adult offspring of predator-exposed mothers and control mothers to a simulated predator attack and measured circulating cortisol at multiple time points. Similarly I compared the cortisol responses between sticklebacks in two different social environments (alone or in a group), and between the sexes. The cortisol response curve differed between offspring of control and predator-exposed mothers, between females and males, and between fish alone and fish in a group. There was no interaction between the social environment and maternal treatments, sex and maternal treatment, or social environment and sex. Altogether these results show that, by some mechanism, maternal exposure to a predator influences development of the stickleback HPI axis. It is likely that activation of the HPI axis in female sticklebacks exposed to stressful events during oogenesis exposes her eggs to elevated cortisol and that her eggs take up some of that extra cortisol. The observation that stickleback mothers exposed to a predator lay eggs with higher cortisol levels is consistent with this idea, though whether stickleback eggs take up cortisol based on the concentration of their surroundings has not been tested. Therefore in the second chapter of my thesis (Chapter 3) I tested the hypothesis that exogenous hormones passively diffuse into eggs. I reviewed the literature on experimental immersion of fish eggs into steroids and found that exogenous glucocorticoid and sex steroids diffuse into both fertilized and unfertilized fish eggs. I also immersed unfertilized stickleback eggs in cortisol and testosterone and measured their levels after exposure. The data confirm that stickleback eggs also exhibit a pattern of diffusion depending on their surrounding concentration, and confirm that the transfer of maternal hormones via diffusion is a potential mechanism underlying the maternal effect in sticklebacks. Finally, the fact that stickleback mothers’ experiences with a predator affect the HPI responsiveness of their adult offspring despite the absence of maternal care in the species indicates that, in early stickleback embryos, the developing HPI axis and brain remain sensitive to maternal stress. In the final chapter of my thesis (Chapter 4) I uncover some of the molecular mechanisms by which maternal predator exposure influences offspring development. A comparison of genome-wide transcription patterns between embryos from predator-exposed and control mothers demonstrates that early stickleback embryos have a significant transcriptomic response to maternal stress. Developmental pathways involved in metabolism, growth, epigenetics, neural development, sexual maturation, and a role for microRNAs were all identified. In conclusion, the data I obtained in my PhD research identifies a non-genetic maternal effect on the physiological stress response of offspring, a probable neuroendocrine mechanism whereby stickleback mothers transmit information about the presence of predators in the environment to their offspring, and a set of molecular mechanisms whereby this information, once received by developing offspring, influences their phenotype non-genetically.

Graduation Semester

2013-08

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Copyright 2013 Brett Mommer

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