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Biology

Evolution of the opercle: changing bones reflect marine/freshwater divide

A tale of two cities: marine and freshwater environments

Fish are found in many different types of habitats, but a major transition that divides them is the one between marine and freshwater environments.  Fish that live in the salty oceans and seas have very different physiological tolerances than fish that live in lakes, ponds, and rivers.  However, their physiology isn’t the only difference that separates them – key aspects of their shape and behavior are also different.  In sticklebacks, for example, an oceanic ancestor has repeatedly invaded various lake habitats in British Columbia and Alaska.  This shift in habitat is often accompanied by a loss of body armor, bony overlapping plates along the fish’s flank, and a reduction or loss of pelvic and dorsal spines.  In many fish species, including stickleback, icefish, and cichlids, changes in environment or diet are often correlated with differences in the opercle, the bony outer structure that primarily protects the sensitive and crucially important gills [Fig 1].  Often, that change involves a stretching of the opercle towards the tail end of the body. The current study focused on opercle evolution in the primarily marine catfishes of the group Ariidae [Fig 2].  These fish live in saltwater, brackish, and freshwater environments across tropical South America.

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Fig 1: A pike with both its opercle bones spread away from the gills (Source: public commons).

Re-constructing catfish relationships

The authors sampled 263 individuals of twenty-two species of Ariidae across three types of environments: saltwater, freshwater, and brackish.  These samples were obtained from sites in Venezuela and Panama.  The researchers collected tail fin samples for DNA analysis and harvested the entire opercle from each fish.  The DNA samples were sequenced for a particular mitochondrial gene, ATPase 6/8, that has been used previously to assess species relationships in other lineages.  These sequences were then used to construct a phylogenetic tree, a branching diagram that reflects the relationships between the individuals or lineages – much like a family tree, but spanning across lineages of organisms rather than individuals in a family.

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Fig 2: A catfish from the Ariidae family (Taken from Stange et al. 2016).

Assessing bone shape

In order to measure shape differences between the opercles of different fish, Stange and colleagues used a technique called geometric morphometrics.  Geometric morphometrics involves placing digital dots, called landmarks, on pictures of the opercle [Fig 3].  The key is that each landmark should be placed on a readily distinguishable and unique position on each individual specimen.  For example, if you wanted to assess the shape of your hand, you might place landmarks on the tip of each finger and on every knuckle.  You want to be able to minimize any variation in the placement of your landmarks so that any differences you see truly reflect changes in shape between specimens, rather than random error when placing landmarks.  The analysis uses the (x,y) coordinates of each landmark across all of the specimens to build a picture of the major axes of variation in shape.

Fig 3: An example of a catfish opercle with the landmarks used in the study. The big, bold landmark (lower left corner of the specimen) is the kind described above. The smaller landmarks are known as semilandmarks and are used to assess the shape of a curve. (Taken from Stange et al. 2016).

Results

Different environments were correlated with significantly different opercle shapes [Fig 4].  There was a clear separation between marine, freshwater, and brackish samples along the major axes of shape variation [Fig 4A].  These differences translated to conspicuously different opercle shapes [Fig 4B].  These data demonstrate the correlation between habitat and opercle shape; however, the adaptive significance of these changes (i.e., what the fish stands to gain from them) remains unclear.

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Fig 4: A) Different environments separated quite cleanly along the major axes of shape variation; blue dots reflect marine samples, green reflect freshwater, and yellow reflect brackish. B) Representative opercle shapes of marine (blue) and freshwater (green) samples. (Taken from Stange et al. 2016).

Conclusions

The current study verifies some previous findings about opercle evolution in stickleback and icefish, demonstrating a similar trend in the evolution of this bone’s shape between freshwater and marine habitats across these lineages.  Consistent and predictable trends in evolution across different lineages usually suggest that such evolution is adaptive – that is, it has a concrete function that impacts the organism’s ability to survive and reproduce under different conditions.

The opercle’s adaptive significance is clear in the case of cichlids, where it is closely associated with various diets, and in sunfish, where it has evolved to be a dramatically shaped and colored exterior bone which functions in mate choice during reproduction.  However, little is known about the adaptive significance of the opercle to fresh and salt water habitats.  It may be that the opercle itself has no adaptive significance, but instead shares genes with other traits that do, and is therefore riding on those traits’ coattails, so to speak.  Still, this study represents a step forward in understanding the drastic transition between fresh and saltwater environments, and raises new questions for future study.

Source

Stange, M., Aguirre‐Fernández, G., Cooke, R. G., Barros, T., Salzburger, W., & Sánchez‐Villagra, M. R. (2016). Evolution of opercle bone shape along a macrohabitat gradient: species identification using mtDNA and geometric morphometric analyses in neotropical sea catfishes (Ariidae). Ecology and Evolution. doi: 10.1002/ece3.2334

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