Document Type

Dissertation

Degree

Doctor of Philosophy (PhD)

Major/Program

Biology

First Advisor's Name

Philip Stoddard

First Advisor's Committee Title

Committee chair

Second Advisor's Name

Danielle McDonald

Second Advisor's Committee Title

Committee member

Third Advisor's Name

Jamie Theobald

Third Advisor's Committee Title

Committee member

Fourth Advisor's Name

Jeremy Chambers

Fourth Advisor's Committee Title

Committee member

Fifth Advisor's Name

Lidia Kos

Fifth Advisor's Committee Title

Committee member

Keywords

Animal communication, Thyroid hormones, Energetic cost, Cellular metabolism, Trade-off, Immune response, Na⁺/K⁺-ATPase, Gene expression

Date of Defense

11-8-2021

Abstract

Understanding how organisms allocate limited resources across physiological systems is a major challenge in biology. This study revealed that high energetic demand of electric signals of male electric fish (Brachyhypopomus gauderio) is matched by a metabolic trade-off with other cellular functions. We used thyroxine (T4) to modulate the fish’s signal metabolism, partitioned the energy budget pharmacologically, and measured energy consumption using oxygen respirometry. In males, total energy consumption was unchanged pre- and post-T4 treatment, while signal metabolism rose and the standard metabolic rate fell in an even trade-off. Total metabolism in females did the opposite. Under T4, the non-signal resting metabolism rose while the signal metabolismfell. These results reveal sex differences in metabolic trade-offs between signaling and cellular metabolism in electric fish and suggest that thyroid hormones regulate the allocation of energy between electric signals and somatic maintenance in favor of reproduction.

To determine whether electric fish trade-off reproduction against innate immunity, as is common in vertebrates, we assessed changes in the bactericidal activity of plasma in B. gauderio challenged with bacterial lipopolysaccharide (LPS), before and after T4 treatment. Females did not modulate innate immunity with any of the treatments, while males elevated bactericidal activity of plasma by about a third following LPS injections, T4 implants, or both together, relative to sham treatment. This outcome was unexpected given that T4 increases the energy consumed by the male’s reproductive electric signals while lowering the rest of his metabolism. T4 also increased expression of Na+K+ATPase pump mRNA in the electrogenic cells of males but not females, consistent with previous findings that T4 differentially regulates signal metabolism in the two sexes. This sex difference in gene regulation suggests Na+K+ATPase underlies sexual dimorphism in electric signal energetics. The results provide further evidence that thyroid hormones play an essential role in the differential allocation of energy among metabolic functions.

This body of work is the first to quantify an energetic trade-off between reproductive behavior and other metabolic functions. and implicates ion pumps, but not innate immunity, as molecular mechanisms underlying sex differences found in these energetic trade-offs.

Identifier

FIDC010437

ORCID

https://orcid.org/0000-0001-5535-7638

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