Martin Luehrmann: Evolution of colour vision in coral reef fishes

Martin Luehrmann is a recent Ph.D. graduate at the University of Queensland in Australia. Here, Martin discusses with us his paper “Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae)”, as well as his interest in ecology and his hobbies outside of research.

What is the background behind your paper?

Intuitively, understanding the proximate and/or ultimate causes for the dynamics of colour vision evolution may seem trivial. However, today, after decades of research and a steadily improved understanding of the physiology and molecular biology underlying colour vision, the selective forces that shaped colour vision evolution and function in the phenotype remain largely unknown in most animals.

A good example to illustrate this is the presence or absence of trichromacy – the ability to distinguish colours based on photoreceptor sensitivities to red, green and blue light, in primates. Even in this group of animals that includes us humans, the causes for red colour vision or the lack thereof remain elusive. Some argue the ability to see red has evolved because it aids a frugivorous diet by improved discrimination of ripe (red) from unripe (green) fruit. Others argue this trait has evolved due to it allowing individuals to identify emotional states or socio-sexual signals via the hue of a conspecific’s skin.

Identifying the selective forces determining the evolution of colour vision thus is the broader incentive behind this paper. Specifically, as part of an effort to understand these dynamics in vertebrates, this paper sought to explore the impact of a possible selective force on colour vision evolution vertebrates in one of the most diverse and colourful ecosystems on earth: coral reefs.

Fish are an ideal candidate to study colour vision evolution in vertebrates for several reasons. One, they constitute the most diverse clade among vertebrates. Two, they boast the widest range of photoreceptor spectral sensitivities among vertebrates, ranging from ultraviolet to red. Three, their natural habitat is subject to significant changes in light due to effects such as light attenuation with increasing depth.  

How is your paper new or different from other work?

It is well established, at the molecular and the physiological level, that overall fish visual systems are tuned to those wavelengths of light available and dominant in their immediate environment. For example, in adaptation to increasingly blue-shifted light at depth due to light attenuation, deep sea fishes show blue-shifted photoreceptor spectral sensitivities compared to shallow water species. Many freshwater habitats, on the other hand, show red-shifted light environments due to organic matter load, as do coastal marine waters compared to pelagic zones. Fish visual systems have adapted to these light conditions. This principle, when first discovered, largely applied only to large scale habitat differences, such as those observed in pelagic versus coastal habitats. A growing number of studies has since shown that these effects may also be present on smaller scales, e.g. between different river zones, types of substrate, or structurally distinct parts of kelp forests. However, the spatial scale that we investigated in this study – some partitions being only centimetres apart, e.g. fish hovering just above the tips of a branching coral compared to fish hiding between those branches – is virtually unprecedented. Our findings provide further clues as to how diverse and structurally complex ecosystems may sustain species richness also through sensory adaptation.

Where you surprised by any of your results?

Microhabitat aggregation behaviour in a handful of cardinalfishes described prior to this study, along with opsin gene expression profiles I identified throughout my PhD, suggested that cardinalfishes show a more blue-shifted opsin repertoire the more exposed their microhabitat was, and a more red-shifted opsin repertoire the more hidden their microhabitat was. While, overall, this trend proved to be true, I was surprised to find that the complete picture was more complex than I had hypothesized, and that in its purest form my prediction applied only to those species that inhabited microhabitats at either end of the chromatic and brightness spectrum. The majority of species showed opsin repertoires and expression patterns suggesting adaptation to intermediate conditions. This, of course, makes perfect sense from an evolutionary perspective when assuming decreased selective pressure on genes serving intermediate wavelengths compared to genes subserving the shorter and longer wavelengths.

Moreover, one species seemed to run against the identified trend entirely. This species occurred in exposed microhabitats and expressed long-wavelength sensitive opsin which was absent in all other non-hidden species. What function may long wavelength sensitivity have in this species?

Does this article raise any new research questions?

It does indeed! On the one hand, these results raise the question of what aspects associated with microhabitat-separated life most influence evolution and function of colour vision in these animals. Though the most prominent candidate answer to this question may be shifts in light between different microhabitats (brightness and/or colour), other aspects of life within these ecosystems and communities may also be important. For example, to what extent does body coloration influence colour vision? This could have implications for con-specific recognition, e.g. in social contexts such as group formation or mating, or for recognising predators or prey.

On the other hand, we wonder whether the effect observed in cardinalfishes is present also in other reef fish families. Could it, perhaps, be specific to fish that display similar levels of site fidelity during relevant times of the day?

It is obvious, however, that as a whole, there remains much to be learned about the functions and evolution of colour vision, not only in fishes, but across all animals.

How did you get involved in ecology?

Born in a small town in Northern Germany, a career in marine science and ecology was not the most obvious path to pursue. However, a lifelong fascination with the outdoors and wildlife, specifically marine life, initially led me to study Biology. Starting in my undergrad at the University of Cologne in Germany, I had the wonderful opportunity to assist Dr. Andrew Nosal at SCRIPPS Institution of Oceanography in San Diego in characterizing the behaviour of a local population of leopard sharks. During further study in Marine Biology at the University of Rostock, Germany, I was given the great opportunity to get involved with Prof. Guido Dehnhardt’s research on marine animal cognition and sensory systems at the Marine Science Center in Rostock, Germany. This led me to undertake a research project at Hagenbeck’s Zoo in Hamburg, Germany, exploring cognitive abilities in zebra sharks. Following these experiences, I sought to broaden my skillset and was fortunate to be able to undertake Ph.D. studies in Prof. Justin Marshall’s visual ecology lab at the University of Queensland, Australia, on the function and evolution of colour vision in reef fishes.

What do you do in your spare time?

I am a big basketball fan. So I play, and also follow the NBA pro scene. During a trip to the USA in 2012, I even managed to watch a game of my favourite team, the Boston Celtics. I also enjoy travelling, to discover foreign cultures and – most of all – the many excellent different foods the world has to offer. Weekends I often spend camping or hiking, and I am an enthusiastic scuba diver, although I wish I could do this more often.

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