Pea Island, NC

Testing the Expensive Tissue Hypothesis

Expectations of energetic trade-offs in oyster toadfish

As part of our ongoing work on teleost neuro-biology I have been obtaining fish samples from various state agencies along the Atlantic Coast. I was picking up samples from Richard Wong at Delaware Fish and Wildlife and we got into a pretty cool conversation about the unusual biology of oyster toadfish.

These fish are wierd. Not only are they one of the few animals we have brought into outer space, but they have the fastest twitching muscles of any vertebrates. Toadfish use these muscles to vibrate a highly modified swimbladder to call to each other. Males take this to the extreme and use an expanded swimbladder to make a boatwhistle call that can be heard at the surface. Not surprisingly, these fishes that like to hang out under docks have been used for physiological experiments for over 100 years and are incredibly well studied. The high levels of investment in unusual physiology in toadfish raised the question of whether there are trade-offs with other organs.

Figure 1. Illustration of an oyster toadfish by Katerina Zapfe

When I got the fish back to the lab our conversation continued and we began to think about how differential changes in organ investment between male and female toadfish might come with hidden costs. I talked to Teresa Iglesias and Dan Warren about their recent paper testing expectations of the ‘expensive tissue hypothesis’ in wrasses..

The expensive tissue hypothesis (ETH) posits that investment in a major metabolically expensive organ, the brain, should come at a cost to one or more other organ systems. As costly traits such as gonads (or in this case massive swim bladders) become expressed, expectations of the ETH suggest that energy budgets will be differentially balanced between sexes. At the extreme this could drive reduced investment in the brain or other structures for the sex under selection. While the ubiquity of trade-offs in life history evolution provides intuitive appeal for the ETH, evidence supporting the expectations of this hypothesis has not been overwhelming.

We decided to see if the ETH holds in toadfish creating what turned out to be a really fun lab project.

Over the course of several weeks, We measured body, brain, liver, swim bladder, heart, and gonad mass in male and female toadfish to test for trade-offs expected by the ETH.

We found clear evidence of a significant change in the allometric slope of swim bladder growth between toadfish sexes. However, our analyses did not recover any evidence of a correlated trade-off in the mass of another organ during ontogeny (See images below). Male toadfish swim bladder mass has previously been found to be highly correlated with both sonic muscle size and the number of fibers making swim bladder mass a good proxy for the heavy energetic cost associated with the development of the male toadfish acoustic repertoire.

We also found no evidence for the expectations of the ETH in female gonad size. This was surprising as, relative to other teleost fish, female toadfish invest an incredible amount of protein into each egg.

This adds our study to the growing number of studies that have failed to recover support for the ETH in traits where an expectation of positive evidence is reasonable (reviewed in Warren & Iglesias, 2012).

While the ETH holds promise of a general evolutionary principle, evidence for direct trade-offs between the brain and other metabolically expensive organs has been limited to few clades. In contrast, numerous studies, including ours, have reported negative evidence. We argue in our manuscript that refinement of the ETH as well as the formulation of new metabolic investment hypotheses is warranted and needed to broaden our perspective on energetic trade-offs.

We don’t argue against the ETH, but it is striking that much of the evidence comes from carefully controlled lab experiments. This suggests that while trade-offs are probably real, wild animals have evolved strategies to mitigate the energetic costs of exaggerated traits. Expanding beyond the ETH is likely to herald some really fundamental insights into the relationship of energetic trade-offs, ecology, and sexual selection in shaping other aspects of organismal form.

Interested in more detail? You can check out our resulting manuscript here!

Dialogue & Discussion