Unsuitable habitat patches lead to severe underestimation of dynamics and gene flow in a zooplankton metapopulation.

Migration and re-colonization enable organisms to persist in metapopulations. Re-colonization success may be limited by the number of arriving migrants or by patch quality. In a well-studied rock pool Daphnia metapopulation, it is frequently assumed that re-colonization is limited by the number of arriving migrants, and that all patches are equally suitable for colonization. This assumption strongly influences how observations about dynamics, epidemiology and population genetics for the entire metapopulation are interpreted. Here we test this assumption. In 627 rock pools, we found that high pH, high Ca(++) and high water conductivity were positively correlated with the presence of D. magna. The experimental release of D. magna into randomly chosen natural pools revealed the highest colonization success in pools with high pH. Next, we elevated pH and Ca(++) concentrations in natural pools by adding a system-specific natural source of calcium carbonate (either from crushed oyster shells or from eider duck droppings, which contain blue mussel shells). These treatments led to a rapid increase in pH and Ca(++) and strongly raised the likelihood that introduced D. magna would establish persistent populations. Therefore, we conclude that low pH and Ca(++) result in unsuitable colonization conditions in two-thirds of the untreated pools. A further experiment revealed that natural colonization rates were about five times higher in calcium-treated pools than in untreated pools. Finally, we observed that eider droppings are more frequently found in the catchment area of occupied pools, than they are in those of unoccupied pools, suggesting that the blue mussel shells contained in the eider droppings play an important role in making pools suitable for colonization and in enabling D. magna to persist. Thus, eider ducks are ecosystem engineers in this system. We recalculate typical metapopulation parameters to account for the unsuitable pools, resulting in a much more dynamic picture of this metapopulation than previously believed, with colonization rates and gene flow three to five times higher. These results have strong implications for metapopulation persistence, local and global genetic diversity, genetic rescue, gene flow and local adaptation. Our results emphasize that without verifying patch suitability, estimated rates of metapopulation dynamics can severely underestimate the true rates.

Converging seasonal prevalence dynamics in experimental epidemics.

BACKGROUND: Regular seasonal changes in prevalence of infectious diseases are often observed in nature, but the mechanisms are rarely understood. Empirical tests aiming at a better understanding of seasonal prevalence patterns are not feasible for most diseases and thus are widely lacking. Here, we set out to study experimentally the seasonal prevalence in an aquatic host-parasite system. The microsporidian parasite Hamiltosporidium tvärminnensis exhibits pronounced seasonality in natural rock pool populations of its host, Daphnia magna with a regular increase of prevalence during summer and a decrease during winter. An earlier study was, however, unable to test if different starting conditions (initial prevalence) influence the dynamics of the disease in the long term. Here, we aim at testing how the starting prevalence affects the regular prevalence changes over a 4-year period in experimental populations. RESULTS: In an outdoor experiment, populations were set up to include the extremes of the prevalence spectrum observed in natural populations: 5% initial prevalence mimicking a newly invading parasite, 100% mimicking a rock pool population founded by infected hosts only, and 50% prevalence which is commonly observed in natural populations in spring. The parasite exhibited similar prevalence changes in all treatments, but seasonal patterns in the 100% treatment differed significantly from those in the 5% and 50% treatments. Populations started with 5% and 50% prevalence exhibited strong and regular seasonality already in the first year. In contrast, the amplitude of changes in the 100% treatment was low throughout the experiment demonstrating the long-lasting effect of initial conditions on prevalence dynamics. CONCLUSIONS: Our study shows that the time needed to approach the seasonal changes in prevalence depends strongly on the initial prevalence. Because individual D. magna populations in this rock pool metapopulation are mostly short lived, only few populations might ever reach a point where the initial conditions are not visible anymore.

Genetic diversity and genetic differentiation in Daphnia metapopulations with subpopulations of known age.

If colonization of empty habitat patches causes genetic bottlenecks, freshly founded, young populations should be genetically less diverse than older ones that may have experienced successive rounds of immigration. This can be studied in metapopulations with subpopulations of known age. We studied allozyme variation in metapopulations of two species of water fleas (Daphnia) in the skerry archipelago of southern Finland. These populations have been monitored since 1982. Screening 49 populations of D. longispina and 77 populations of D. magna, separated by distances of 1.5-2180 m, we found that local genetic diversity increased with population age whereas pairwise differentiation among pools decreased with population age. These patterns persisted even after controlling for several potentially confounding ecological variables, indicating that extinction and recolonization dynamics decrease local genetic diversity and increase genetic differentiation in these metapopulations by causing genetic bottlenecks during colonization. We suggest that the effect of these bottlenecks may be twofold, namely decreasing genetic diversity by random sampling and leading to population-wide inbreeding. Subsequent immigration then may not only introduce new genetic material, but also lead to the production of noninbred hybrids, selection for which may cause immigrant alleles to increase in frequency, thus leading to increased genetic diversity in older populations.

Strong inbreeding depression in a Daphnia metapopulation.

The deleterious effects of inbreeding have long been known, and inbreeding can increase the risk of extinction for local populations in metapopulations. However, other consequences of inbreeding in metapopulations are still not well understood. Here we show the presence of strong inbreeding depression in a rockpool metapopulation of the planktonic freshwater crustacean Daphnia magna, which reproduces by cyclical parthenogenesis. We conducted three experiments in real and artificial rockpools to quantify components of inbreeding depression in the presence and the absence of competition between clonal lines of selfed and outcrossed genotypes. In replicated asexual populations, we recorded strong selection against clones produced by selfing in competition with clones produced by outcrossing. In contrast, inbreeding depression was much weaker in single-clone populations, that is, in the absence of competition between inbred and outbred clones. The finding of a competitive advantage of the outbred genotypes in this metapopulation suggests that if rockpool populations are inbred, hybrid offspring resulting from crosses between immigrants and local genotypes might have a strong selective advantage. This would increase the effective gene flow in the metapopulation. However, the finding of low inbreeding depression in the monoclonal populations suggests that inbred and outbred genotypes might have about equal chances of establishing new populations.

A selective advantage to immigrant genes in a Daphnia metapopulation.

Immigrants to habitats occupied by conspecific organisms are usually expected to be competitively inferior, because residents may be locally adapted. If residents are inbred, however, mating between immigrants and residents results in offspring that may enjoy a fitness advantage from hybrid vigor. We demonstrate this effect experimentally in a natural Daphnia metapopulation in which genetic bottlenecks and local inbreeding are common. We estimate that in this metapopulation, hybrid vigor amplifies the rate of gene flow several times more than would be predicted from the nominal migration rate. This can affect the persistence of local populations and the entire metapopulation.