From the bare minimum

Can too much relatedness affect the fate of pioneers?

In a previous post, we spoke about how brown trout managed a rather successful colonization of the remote sub-Antarctic Kerguelen Islands. We also believe that multiple introductions in different river systems and from different origins in Europe increased the probability of success in this process (Lecomte et al. 2013). The general idea behind this belief is that more diversity allows for faster adaptation over generations (or simply allows to select the most adapted genotype at introduction). This well accepted idea in evolutionary biology and in invasion biology can also be looked the other way around: a total lack of genetic variation should actively prevent selection, and thereby possibly prevent adaptation, persistence, and further successful colonization. Think of two genitors, one male, one female, arriving together in a virgin river, and mating there for the first time: the river is initially (and possibly eventually) populated in the most inbred way: brothers and sisters. That means, hell of a low genetic diversity. But it could actually be a frequent case during a colonization process.

A map of Kerguelen Islands where we can observe that much of the eastern parts have been colonized. Our two populations of Val Travers and Clarée, however, are located on the western colonization front.

It is not easy to actually monitor such things naturally, one has to be very lucky to be there, at the right place, at the right time. Although such a luck may sometimes occur, we have another way to look at such a scenario: in the colonization process of Kerguelen, some remote sites were introduced by man as late as 1993, and for two of them, Val Travers and Clarée, we have the initial number of parents that were used to generate the progenies for introduction (one female and one male for Val Travers, one female and two males for Clarée). These two systems have another characteristic: they are still far away from other colonized rivers, and so we can be fairly certain that no immigration occurred yet. 

  At the top, a view of the Val Travers valley, typically stemming down from moutains, with various small tributaries offering variable habitats for all developmental stages. The river then mouthes into the Lake Bontemps, where some adults thrive on plankton, and they may also migrate to sea, but will not come back due to a seemingly impassable outlet. At the bottom, a view of the Clarée system: this network of river arms is located downstream a cold long lake, but also receives water from a glacier tributary. The network itself is complex and constantly changing, but its length is reduced (3km) before mouthing in the the marine bay of Radioleine. Habitats are homogeneous at best, but constant plankton delivery is ensured by the upstream lake.

So we came to sample these systems in 2003, ant it appeared that they were populated, and we could observe that not only local reproduction occurred, but many individuals were in fact pioneers (the ones released in 1993 as fry). In 2010, we sampled again theses systems, and we could see that both were hosting relatively thriving populations. Each time, we sampled scales: they allow to age each fish, and they can also serve to obtain their genotype. Each fish was genotyped using microsatellite markers in order to measure their individual homozygosity level: at each locus, if the two alleles are similar, this locus is deemed homozygous (versus heterozygous if alleles differ). Roughly, Homozygosity Level (HL) generalizes the proportion of loci that are homozygotes within an individual. Under strong inbreeding (say the Val Travers situation), the first generations are expected to be highly homozygous, simply because for each locus, only 4 alleles at most are available, and there is therefore a rather high probability to have identical alleles. Being homozygous can be detrimental for fitness since potential deleterious mutations are then fully expressed. HL therefore gives an idea of the risk for an individual to express deleterious mutations, and to consequently suffer a reduced fitness. Let’s have a look at the distribution of HL in each population for the two sampling dates:

Distribution of Homozygosity Level for each population at each sampling dates. A 1 value means a fully homozygous individual.

 

It appears that Val Travers shows higher values of HL, which is logical if we remind that this population was founded by two parents, against 3 for Clarée. We can also observe that the higher values of HL present in 2003 are not found in 2010 in Val Travers, as if these individuals had disappeared. For Clarée, this is nearly he opposite, but this could be due to a lower sample size in 2003.

In order to check if HL had an effect on survival, we used age as a proxy of survival, hoping that the distribution of age would not be independent from the distribution of HL: if homozygosity is detrimental to survival, aged individuals should have lower than average value of HL.

The results are somewhat puzzling: our hypothesis was confirmed in the Val Travers population, with rather strong and durable selection against highly homozygous individuals. But in Clarée, we failed to detect a consistent selection against the most homozygous individuals. Interestingly, we were also able to derive variation in inbreeding within each population: in Val Travers, we found a large variance, meaning that all individual did not have the same level of inbreeding. In Clarée however, this variance was close to zero: all individuals appear to share the same level of inbreeding, which provides little room for selection to distinguish between them, if inbreeding is the conveyor of deleterious mutations. 

Relationship between Age at capture (as estimated from scales) and Homozygosity Level (HL) in the Val Travers population. The various points and curves show different adjustments of models for the dates (2003 and 2010) and for the two sexes.

The morale of this story could be that, during colonization, with very little genetic variation and important inbreeding, very different outcomes can be expected, and inbreeding or reduced genetic variation may not be a problem, and may not always prevent selection to act. In any case, these two populations persisted and keep on growing nowadays, they are possibly on the verge of colonizing new river systems.

The details of the story however are for more complex: the initial genes differ between the two environments, and our estimation of inbreeding relies on microsatellite loci, which are known to mutate rapidly, a process that could easily shadow the true role of inbreeding for functional genes (which mutate more slowly). More details and discussion can be found in our original paper in Evolutionary Ecology Research. 

Labonne J., Kaeuffer R., Guéraud F., Zhou M., Manicki A., Hendry A.P. 2016. From the bare minimum: genetics and selection in populations founded by only a few parents. Evolutionary Ecology Research, 17:21-34.

Lecomte, F.; Beall, E.; Chat, J.; Davaine, P.; Gaudin, P. 2013. The complete history of salmonid introductions in the Kerguelen Islands, Southern Ocean. Polar Biology, 36 (4) : 457-475.