Eutrophication causes speciation reversal in whitefish adaptive radiations

Following the retreat of the ice after the Würm ice age in Central Europe some 10,000 years ago, Alpine-, and pre-Alpine lakes were colonized by a hybrid swarm of whitefish. These whitefish subsequently sympatrically radiated in parallel into a number of distinct ecotypes in multiple lakes resulting in the existence of between one and six genetically and phenotypically distinct whitefish species within the lakes. Whitefish in general and in this study system in particular have become a key study organism in our studies on adaptive radiation and ecological speciation. Since whitefish are keystone- and dominant planktivores, the system shows great potential for studying eco-evolutionary dynamics and possibly feed-backs.

However, as a result of anthropogenic eutrophication during the last century of almost all larger Alpine and pre-Alpine lakes, whitefish diversity became threatened. In the recent issue of Nature, Pascal Vonlanthen and co-workers show that this eutrophication has led to species loss through speciation reversal. The mechanism responsible for this species reversal is likely limited egg survival in the sediment caused by low oxygen concentration at larger depths as a result of bacterial decomposition of increased organic matter following the eutrophication process. This has differential effects on different species of whitefish, since whitefish diversity to a large extent is maintained by spawning segregation by depth. Diversity loss can happen through two different processes, namely demographic decline and speciation reversal through introgressive hybridization. Vonlanthen and his co-workers show evidence of at least the latter, which is illustrated by decreasing pairwise FST-values between sympatric species pairs. In one specific case, private alleles that were found in a species that went extinct during the eutrophication period are now found in contemporary species.

Eutrophication has especially in industrialized countries been replaced by re-oligotrophication and so also around the Alps of Central Europe. After phosphorous removal in waste water treatment became more efficient and phosphorous in washing detergents was banned, at least in Switzerland, the lakes are returning towards their original state and sediment surfaces start to be oxygenated again throughout the depth range. However, the species diversity was not restored. Thus, the study contributes to the growing body of evidence that not only species diversity should be targeted by conservation goals, but also the processes, like adaptive radiation, that are generating new diversity  should be taken into consideration, which is not the case in most current management programs.

An important question arising from the study is whether we can expect ecosystem dynamics and functioning to return to historic states, when phenotypic diversity has been diminished. Will the trophic transfer rates in the planktonic food web decrease when the most efficient planktivores have been lost? And will utilization of profundal resources disappear or will other species be able to invade these niches before whitefish once again radiate into new distinct phenotypes? But the study also raises interesting questions regarding the process of speciation reversal in it self especially concerning why historically private alleles of species going extinct become introgressed into surviving species. Is the hybridization leading to this process a result of phenotypic plasticity in spawning habitat or time, where previously deep-water spawning species changed their habits and spawned at shallower depths and thereby overlap with other spawning whitefish? Or has a fraction of the distinct species always hybridized, with hybrids historically being selected against due to disruptive selection? In either case, this paper has given us a lot to think about.

The paper:

P. Vonlanthen, D. Bittner, A.G. Hudson, K.A. Young, R. Müller, B. Lundsgaard-Hansen, D. Roy, S. Di Piazza, C.R. Largiader & O. Seehausen (2012). Eutrophication causes species reversal in whitefish adaptive radiation. Nature, 482: 357-362.