How does evolution shape bones and muscles that are used in multiple biomechanical systems ? This question has inspired my interest in fish gill ventilation. Gill ventilatory pumping in fishes requires the use of more than 20 individual bones and 8 distinct muscles, most of which are also used in feeding and other behaviors. This overlap in structures among functions is known as "functional coupling," which is thought to constrain morphological evolution. However, fish skulls are incredibly diverse. Is functional coupling really so constraining after all? If so, are there mechanisms for relaxed constraint in some lineages, allowing them to become morphologically diverse? These are the questions that I hope to answer in my research. Check out my Google Scholar profile and the descriptions below to read about my work.

The basics of fish gill ventilation

Ray-finned fishes (Actinopterygii) ventilate their gill tissue by pumping water into the mouth, over the gills, and out the gill openings. This allows water to flow in a single direction over the microstructures of the gills, setting up a countercurrent gas exchange system with the bloodstream, which flows through the respiratory tissue in the opposite direction.

However, getting water to flow in one direction is not so easy. To do this, fishes take advantage of the fact that fluids move from areas of high pressure to low pressure. They use cyclical pumping of the mouth and gill chambers (Figs. 1 and 2), which are expanded and compressed by many bones and muscles. Expansion of a chamber generates negative pressure, and compression of a chamber generates positive pressure. Check out the animation (Fig. 2) to see the pattern of flow through a fish skull.

The fish that breathes out its armpit. 

We can learn a lot about the evolution of a biomechanical system by studying extreme cases— animals that "break the rules." For gill ventilation, the Goosefish (Lophius americanus) is a great example of this, because they breathe incredibly slowly. Goosefish are bottom-dwellers that blend in with the sandy ocean floor and ambush prey. They are anglerfishes, and therefore they have a lure for attracting prey (Fig. 3). You may have eaten a goosefish - they are called "monkfish" in the culinary world!  

An average goosefish takes over a minute to complete one ventilatory cycle (Farina and Bemis, 2016), and bigger goosefish take even longer (up to 5 minutes)! This is more than 100 times slower than a goldfish! This makes it much easier for them to hide their ventilatory movements from predators and prey. Their slow breathing is possible only because of their gigantic gill chambers, which extend underneath the pectoral fins and end with the gill opening positioned in the "armpit" of the fish (Fig. 3). They have specialized musculature, which we describe in our paper, to hold the gill opening in a siphon-like shape during exhale. Watch the video below to see this in action!

Farina, SC, WE Bemis. 2016. Functional morphology of gill ventilation in the Goosefish, Lophius americanus (Lophiiformes: Lophiidae). Zoology. 119:207-215.

Evolution of gill ventilation

So how does the goosefish help us to understand such a complex system shared by all 30,000+ species of ray-finned fishes? Their gill chambers are highly specialized in two ways: they have extremely elongate branchiostegal rays and a small gill opening. I have investigated the function and evolutionary history of both of these adaptations across ray-finned fishes.

I completed a large-scale phylogenetic survey of gill opening morphology across 433 families of ray-finned fishes. My co-authors and I found that tiny, restricted gill openings have evolved independently more than 20 times in at least 11 major clades. We found that fishes with restricted gill openings repeatedly occur under a variety of ecological conditions, although they are rare in open-ocean pelagic environments. We concluded that this specialized gill opening morphology likely evolved for very different functions in different lineages, including providing greater stability of the branchiostegal apparatus, allowing opercular jetting for burial and locomotion, and providing evolutionary flexibility in gill opening position. 

Farina, SC, TJ Near, WE Bemis. 2015. Evolution of the branchiostegal membrane and restricted gill openings in actinopterygian fishes. Journal of Morphology 276:681-694. 

To further explore the evolution and function of the gill ventilatory system, I focused on the Cottoidei (sculpins and relatives), a group of bottom-dwelling fishes with considerable variation in cranial morphology. I measured ventilatory pressures in the mouth and gill chambers of four sculpins and found that pressures differed greatly among species. Much of the pressure variation was explained by the size of the branchiostegals. Branchiostegal rays (see Fig. 1) support the gill chamber and contribute substantially to ventilatory pumping. 

Farina, SC, LA Ferry, M Knope, AP Summers, and WE Bemis. The contribution of the branchiostegal apparatus to driving ventilatory current in cottoid fishes. Society for Integrative and Comparative Biology. West Palm Beach, FL. January 

I then used micro-CT reconstructions to analyze cranial bones in 20 cottoids. I found that the jaws, opercular bones,