Jukka Jokela

Speciation reversal and biodiversity dynamics with hybridization in changing environments

A considerable fraction of the worlds biodiversity is of recent evolutionary origin and has evolved as a by‐product of, and is maintained by, divergent adaptation in heterogeneous environments. Conservationists have paid attention to genetic homogenization caused by human‐induced translocations (e.g. biological invasions and stocking), and to the importance of environmental heterogeneity for the ecological coexistence of species. However, far less attention has been paid to the consequences of loss of environmental heterogeneity to the genetic coexistence of sympatric species. Our review of empirical observations and our theoretical considerations on the causes and consequences of interspecific hybridization suggest that a loss of environmental heterogeneity causes a loss of biodiversity through increased genetic admixture, effectively reversing speciation. Loss of heterogeneity relaxes divergent selection and removes ecological barriers to gene flow between divergently adapted species, promoting interspecific introgressive hybridization. Since heterogeneity of natural environments is rapidly deteriorating in most biomes, the evolutionary ecology of speciation reversal ought to be fully integrated into conservation biology.

The Maintenance of Sex, Clonal Dynamics, and Host‐Parasite Coevolution in a Mixed Population of Sexual and Asexual Snails

Sexual populations should be vulnerable to invasion and replacement by ecologically similar asexual females because asexual lineages have higher per capita growth rates. However, as asexual genotypes become common, they may also become disproportionately infected by parasites. The Red Queen hypothesis postulates that high infection rates in the common asexual clones could periodically favor the genetically diverse sexual individuals and promote the short‐term coexistence of sexual and asexual populations. Testing this idea requires comparison of competing sexual and asexual lineages that are attacked by natural parasites. To date no such data have been available. Here, we report on long‐term dynamics and parasite coevolution in a “mixed” (sexual and asexual) population of snails (Potamopyrgus antipodarum). We found that, within 7–10 years, the most common clones were almost completely replaced by initially rare clones in two different habitats, while sexuals persisted throughout the study period. The common clones, which were initially more resistant to infection, also became more susceptible to infection by sympatric (but not allopatric) parasites over the course of the study. These results are consistent with the Red Queen hypothesis and show that the coevolutionary dynamics predicted by the theory may also favor sexual reproduction in natural populations.

Predator avoidance and immune defence: costs and trade–offs in snails

Organisms are often confronted by both predators and pathogens. Defending against such widely divergent enemies requires more than one type of defence. Multiple defences, however, raise the possibility of trade–offs among defences. We tested for such trade–offs by manipulating the level of predator–avoidance behaviour and immune function in the freshwater snail Lymnaea stagnalis (Gastropoda: Pulmonata). Our results show that predator avoidance and immune function had clear costs in terms of reproduction and survival. Further, we show that increased levels of predator–avoidance behaviour reduced the snails ability to defend against potential pathogens. Predator–avoidance behaviour may thus have the additional indirect cost of reduced immunocompetence and increased susceptibility to pathogens. Our results suggest that ecological factors (e.g. predator density) may considerably modify the expression and costs of immune defences.

Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum)

Larval digenetic trematodes commonly castrate their first intermediate hosts, and should therefore impose strong selection on the timing and mode of host reproduction. Here we examine spatial variation in infection by trematodes in the freshwater snail Potamopyrgus antipodarum. Snails were collected at 11 different sites at Lake Alexandrina on the South Island of New Zealand from transects that ran perpendicular to the shore and across several different habitat types (from 0 to 8 m deep). Logistic regression was used to analyze the relationships between the frequency of trematode infection and snail size, habitat type, and transect location. On average, the probability of infection increased 3.3 times with each 1 mm increase in shell length. Prevalence of infection by the most common species of trematode, Microphallus sp., was highest in the shallow-water habitats where its final hosts (waterflow) spend most of their time. Prevalence of infection by another parasite, Telogaster ophistorchis (final host: eels) increased with depth, but because Microphallus was much more common, total infection by all trematodes decreased with depth. The effects of transect location were minor for Telogaster, but there was significant variation in Microphallus prevalence among transects, especially in the shore-bank habitat. Taken together, these results suggest that the risk of infection is spatially variable, but generally higher in shallow-water habitats, which may explain the greater frequency of sexual individuals as well as earlier reproduction among individuals near shore.

GENETIC STRUCTURE OF COEXISTING SEXUAL AND CLONAL SUBPOPULATIONS IN A FRESHWATER SNAIL (POTAMOPYRGUS ANTIPODARUM)

We examined clonal diversity and the distribution of both clonal and sexual genotypes in a single population of freshwater snails (Potamopyrgus antipodarum) in which diploid sexual individuals and triploid parthenogens coexist. A genetic analysis of individuals from three habitat zones in Lake Alexandrina, New Zealand revealed extremely high clonal diversity: 165 genotypes among 605 clonal individuals. The frequency of triploid clonal individuals increased with increasing depth in the lake, and most of the individual clones were habitat specific, suggesting that differences among habitats are important in structuring the clonal subpopulation. There were also high levels of clonal diversity within habitats, suggesting frequent origins of habitat‐specific clones. In contrast, diploid sexual individuals were proportionately more common in the shallow regions of the lake (where infection by trematode larvae is highest), and there was no significant spatial structure in the sexual subpopulation. We suggest that habitat specialization by clones, as well as parasite‐mediated selection against common clones, are important factors affecting the structure of this mixed population of sexual and clonal snails.

Host Sex and Local Adaptation by Parasites in a Snail-Trematode Interaction

One of the leading theories for the evolutionary stability of sex in eukaryotes relies on parasite‐mediated selection against locally common host genotypes (the Red Queen hypothesis). As such, parasites would be expected to be better at infecting sympatric host populations than allopatric host populations. Here we examined all published and unpublished infection experiments on a snail‐trematode system (Potamopyrgus antipodarum and Microphallus sp., respectively). A meta‐analysis demonstrated significant local adaptation by the parasite, and a variance components analysis showed that the variance due to the host‐parasite interaction far exceeded the variance due to the main effects of host source and parasite source. The meta‐analysis also indicated that asexual host populations were more resistant to allopatric sources of parasites than were (mostly) sexual host populations, but we found no significant differences among parasite populations in the strength of local adaptation. This result suggests that triploid asexual snails are more resistant to remote sources of parasites, but the parasite has, through coevolution, overcome the difference. Finally, we found that the degree of local adaptation did not depend on the genetic distance among host populations. Taken together, the results demonstrate that the parasites are adapted, on average, to infecting their local host populations and suggest that they may be a factor in selecting against common host genotypes in natural populations.

PARASITES, SEX, AND EARLY REPRODUCTION IN A MIXED POPULATION OF FRESHWATER SNAILS

Two hypotheses have been presented regarding the effects of parasites on the life-history evolution of their hosts. First, a high risk of infection should favor sexual reproduction over parthenogenetic reproduction, because sexually produced progeny should be better able to evade coevolving parasites (Levin 1975; Jaenike 1978; Hamilton 1980; Bell 1982; Hamilton et al. 1990; Howard and Lively 1994); this idea has come to be known as the Red Queen hypothesis (see Bell 1982). Second, a high risk of infection is predicted to favor early reproduction, especially if infection results in host castration or death (Gadgil and Bossert 1970; Law 1979; Michod 1979; Minchella and Loverde 1981). The evidence from comparative studies have been generally favorable to both the Red Queen hypotheses (Lively 1987, 1992; Schrag et al. 1994) and to the predictions of life-history theory (Lafferty 1993). These studies have focused on comparing data from different populations of aquatic gastropods. In the present study, we examined the predictions of these theories in a single population of freshwater snails (Potamopyrgus antipodarum), which contains a mixture of obligately sexual and obligately parthenogenetic females. The results were in agreement with both theories.

Increasing water temperature and disease risks in aquatic systems: Climate change increases the risk of some, but not all, diseases

Global warming may impose severe risks for aquatic animal health if increasing water temperature leads to an increase in the incidence of parasitic diseases. Essentially, this could take place through a temperature-driven effect on the epidemiology of the disease. For example, higher temperature may boost the rate of disease spread through positive effects on parasite fitness in a weakened host. Increased temperature may also lengthen the transmission season leading to higher total prevalence of infection and more widespread epidemics. However, to date, general understanding of these relationships is limited due to scarcity of long-term empirical data. Here, we present one of the first long-term multi-pathogen data sets on the occurrence of pathogenic bacterial and parasitic infections in relation to increasing temperatures in aquatic systems. We analyse a time-series of disease dynamics on two fish farms in northern Finland from 1986 to 2006. We first demonstrate that the annual mean water temperature increased significantly on both farms over the study period and that the increase was most pronounced in the late summer (July-September). Second, we show that the prevalence of infection (i.e. proportion of fish tanks infected each year) increased with temperature. Interestingly, this pattern was observed in some of the diseases (Ichthyophthirius multifiliis, Flavobacterium columnare), whereas in the other diseases, the pattern was the opposite (Ichthyobodo necator) or absent (Chilodonella spp.). These results demonstrate the effect of increasing water temperature on aquatic disease dynamics, but also emphasise the importance of the biology of each disease, as well as the role of local conditions, in determining the direction and magnitude of these effects.

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.

Clinal Variation for Local Adaptation in a Host-Parasite Interaction

Using a reciprocal cross-infection experiment, we detected clinal variation in the relative ability of trematodes to infect snails taken from the same habitat. Snails (Potamopyrgus antipodarum) collected from three habitats in a New Zealand lake were exposed to a digenetic trematode (Microphailus sp.) collected from infected snails from the same three locations. The habitats were arranged according to depth, from shallow (the shore bank habitat: less than 1 m deep), to intermediate (the Isòëtes habitat: 1.5-3 m), to deep (the Elodea habitat: 4-6 m). Snails were assayed for infection at two points in the development of the parasite: 4-months post infection (the blastocercariae stage), in which the parasite was not yet infective to the final hosts (ducks), and 7-months post infection (the metacercariae stage), in which the worms were fully encysted and competent for transmission to the final host. At 7-months post infection, the results showed that shallow-water parasites were significantly more infective to shallow-water hosts, but deep-water parasites were about equally infective to snails from all three habitats. This result suggests that gene flow by the parasite is primarily from shallow to deep habitats, and that recycling of the parasite and host-parasite coevolution is primarily in shallow water. Such recycling would be consistent with our observations of foraging by the definitive host of the parasite, and may explain the maintenance of high frequencies of sexual individuals around the shallow-water margins of the lake.