Ole Seehausen talks with
ScienceWatch.com and answers a few questions about
this month's Fast Moving Fronts paper in the field of
Environment/Ecology. The author has also sent along images of
his work.
Article: Speciation through sensory drive in cichlid
fish
Authors: Seehausen, O;Terai, Y;Magalhaes,
IS;Carleton, KL;Mrosso, HDJ;Miyagi, R;van der Sluijs,
I;Schneider, MV;Maan, ME;Tachida, H;Imai, H;Okada, N
Journal: NATURE, 455 (7213): 620-U23 OCT 2 2008
Addresses: Univ Bern, Inst Zool, Baltzerstr 6, CH-3012 Bern,
Switzerland.
Univ Bern, Inst Zool, CH-3012 Bern, Switzerland.
Ctr Ecol Evolut & Biogeochem, Dept Fish Ecol & Evolut,
Eawag, Swiss Fed Inst Aquat Sci & Technol, CH-6047
Kastanienbaum, Switzerland. (addresses have been
truncated.)
Why do you think your paper is highly
cited?
Speciation research is currently one of the most active fields in
evolutionary and ecological research. The cichlid fish of African lakes are
textbook examples of rapid speciation, but the mechanisms of rapid
speciation remain elusive.
Our work on cichlids in Lake Victoria demonstrates the ecological drivers
and molecular basis of divergent evolution of the visual system, which
leads to speciation by a mechanism called "sensory drive" through
interacting natural and sexual selection.
Our paper is perhaps the first case in cichlid fish speciation research
where nearly the complete cascade of interacting mechanisms during
speciation, as well as the temporal sequence in which they come into
effect, could be addressed. This was possible through investigating
replicate cases of speciation at variable levels of completion.
Our data also speak to the causes of species loss through reversal of
speciation. Combining ecology, population genetics, experimental behavioral
genetics, and molecular biology, the paper may speak to scientists in a
wider range of biological disciplines.
Does it describe a new discovery, methodology, or
synthesis of knowledge?
It describes new discoveries and integrates these with previous knowledge.
The central theme of our paper is the demonstration that sympatric
populations, which live at different water depths and had evolved different
male breeding coloration, had also undergone divergent evolution in their
visual pigments, adapting to the local light and matching the male breeding
coloration.
The male breeding color
phenotypes...
Variation in the
divergence
between...
Driving the process of speciation, this adaptive divergence preceded
differentiation at neutral genetic markers.
Would you summarize the significance of your paper
in layman's terms?
Theoretically, adaptation of sensory and signaling systems to local
environmental signal transmission conditions can cause speciation when the
sensory or signaling systems affect mate choice. This is called "sensory
drive speciation."
However, empirical evidence is rare and incomplete. Speciation, in general,
and sensory drive speciation in particular, is thought to usually require
geographical isolation.
In our paper, we demonstrate sensory drive speciation within island
populations of cichlid fish, i.e., without geographical isolation. We
identify the ecological and molecular basis of divergent evolution in the
cichlid visual system, demonstrate associated divergence in male coloration
and female mating preferences for these, and show subsequent
differentiation at neutral genetic markers of gene flow, indicating
reproductive isolation and speciation (Figure 1).
Evidence is replicated in several pairs of sympatric populations, but the
completeness of speciation varies from none to complete (Figure 2).
Interestingly, we could explain when speciation happens and when it does
not.
Variation in how quickly the ambient aquatic light changes with increasing
water depth—slowly in clear water, fast in turbid
water—explains most of the variation in the completeness of
speciation: speciation only occurs in clear water.
Our results also provide a mechanistic explanation for the collapse of
cichlid fish species diversity during the anthropogenic eutrophication of
Lake Victoria when water quickly became turbid.
How did you become involved in this research and
were any particular problems encountered along the way?
I have been working for a number of years on speciation in Lake Victoria
cichlids. In the mid-1990s, during my Ph.D. studies, I found that how
strongly sympatric species were differentiated at different islands
correlated with the clarity of the water. By then I showed that behavioral
reproductive isolation required clear waters.
However, the precise mechanism of speciation, its association with
adaptation to light conditions, and the genes involved remained unknown. I
suspected that evolution in the visual system was the key. I started
collaborating with groups that worked on the genetics of cichlid vision,
Karen Carleton (University of Maryland in College
Park, and Nori Okada (Tokyo Institute of Technology). This was
back in 2001 and 2003. Work on this paper started in 2004 with Nori
Okada's group.
Where do you see your research leading in the
future?
The exact mechanism by which adaptation in the visual system generates
behavioral reproductive isolation is not yet known. This is an area of
active research in my lab.
In collaboration with Martine Maan we investigate the effects on mating
preferences of opsin protein sequence and expression variation, and
other sensory modalities.
My collaboration with Nori Okada and Karen Carleton has broadened to
comparative analyses of visual system evolution in adaptive radiations of
cichlid fish in several lakes.
I have also generalized my approach beyond the specifics of evolution in
the visual system to investigate the role of adaptation to different water
depth in the evolution of fish species diversity more broadly, and the ways
in which environmental variation co-determines when speciation happens and
if species persist.
Do you foresee any social or political
implications for your research?
Yes. Our work demonstrates that, whether or not species persist, and
whether or not speciation happens in the first place, depends on the state
of the environment.
Loss of clear waters is associated with loss of adaptation to the light
conditions at different depth, and with loss of genetic and ecological
differentiation of species, high species diversity that characterizes
African Great lakes can erode within just a few decades of pollution.
We have recently discovered very similar processes in other fish in
European lakes. We are only guessing what ecosystem effects this erosion of
species diversity has, but it is likely that it affects the efficacy of
nutrient cycling and ecosystem resilience, and eventually, ecosystem
services.
I would hope that our work contributes to the raising of an awareness among
resource managers that eutrophication—the excessive increase of
nutrients in a lake or other body of water—the single strongest
impact of man on lakes worldwide, is a major threat to the persistence of
the unique fish diversities found in many lakes.
Importantly—and this is rarely appreciated—the loss of unique
species diversities of lakes is rapid and cannot be repaired by cleaning up
a once-polluted lake! Prevention is the only way to preserve the
diversities of lake fish.
Ole Seehausen
Professor of Aquatic Ecology & Evolution
Division of Aquatic Ecology & Evolution
Institute of Ecology and Evolution
University of Bern
Bern, Switzerland
and
Head of Department Fish Ecology & Evolution
EAWAG Swiss Federal Institute for Aquatic Science and Technology
Centre of Ecology, Evolution and Biogeochemistry
Kastanienbaum, Switzerland Web
KEYWORDS: LAKE VICTORIA CICHLIDS; TUNING SPECTRAL SENSITIVITY; OPSIN
GENE-EXPRESSION; SEXUAL SELECTION; REPRODUCTIVE ISOLATION; MOLECULAR
EVOLUTION; COLOR-VISION; DIVERGENT SELECTION; ADAPTIVE DIVERGENCE;
NATURAL-SELECTION.