Distinct evolutionary lineages of Schistocephalus parasites infecting co-occurring sculpin and stickleback fishes in Alaska.

Sculpins (coastrange and slimy) and sticklebacks (ninespine and threespine) are widely distributed fishes cohabiting 2 south-central Alaskan lakes (Aleknagik and Iliamna), and all these species are parasitized by cryptic diphyllobothriidean cestodes in the genus Schistocephalus. The goal of this investigation was to test for host-specific parasitic relationships between sculpins and sticklebacks based upon morphological traits (segment counts) and sequence variation across the NADH1 gene. A total of 446 plerocercoids was examined. Large, significant differences in mean segment counts were found between cestodes in sculpin (mean = 112; standard deviation [s.d.] = 15) and stickleback (mean = 86; s.d. = 9) hosts within and between lakes. Nucleotide sequence divergence between parasites from sculpin and stickleback hosts was 20.5%, and Bayesian phylogenetic analysis recovered 2 well-supported clades of cestodes reflecting intermediate host family (i.e. sculpin, Cottidae vs stickleback, Gasterosteidae). Our findings point to the presence of a distinct lineage of cryptic Schistocephalus in sculpins from Aleknagik and Iliamna lakes that warrants further investigation to determine appropriate evolutionary and taxonomic recognition.

Cross-continental experimental infections reveal distinct defence mechanisms in populations of the three-spined stickleback Gasterosteus aculeatus.

Epidemiological traits of host-parasite associations depend on the effects of the host, the parasite and their interaction. Parasites evolve mechanisms to infect and exploit their hosts, whereas hosts evolve mechanisms to prevent infection and limit detrimental effects. The reasons why and how these traits differ across populations still remain unclear. Using experimental cross-infection of three-spined stickleback Gasterosteus aculeatus and their species-specific cestode parasites Schistocephalus solidus from Alaskan and European populations, we disentangled host, parasite and interaction effects on epidemiological traits at different geographical scales. We hypothesized that host and parasite main effects would dominate both within and across continents, although interaction effects would show geographical variation of natural selection within and across continents. We found that mechanisms preventing infection (qualitative resistance) occurred only in a combination of hosts and parasites from different continents, while mechanisms limiting parasite burden (quantitative resistance) and reducing detrimental effects of infection (tolerance) were host-population specific. We conclude that evolution favours distinct defence mechanisms on different geographical scales and that it is important to distinguish concepts of qualitative resistance, quantitative resistance and tolerance in studies of macroparasite infections.

Are solo infections of the diphyllobothriidean cestode Schistocephalus solidus more virulent than multiple infections?

We performed a long-term natural experiment investigating the impact of the diphyllobotriidean cestode Schistocephalus solidus on the body condition and clutch size (CS) of threespine stickleback Gasterosteus aculeatus, its second intermediate host, and the growth of larval parasites in host fish. We tested the hypothesis that single S. solidus infections were more virulent than multiple infections. We also asked whether the metrics of mean and total parasite mass (proxies for individual and total volume, respectively) were consistent with predictions of the resource constraints or the life history strategy (LHS) hypothesis for the growth of, hence exploitation by, larval helminths in intermediate hosts. The samples were drawn from Walby Lake, Alaska in eight of 11 years. Host body condition and CS (egg number per spawning bout) decreased significantly with intensity after adjustments for host size and parasite index. Thus, infections have an increasingly negative impact on measures of host fitness with greater intensity, in contrast to the hypothesis that single infections are more harmful than multiple infections. We also found that mean parasite mass decreased with intensity while total parasite mass increased with intensity as predicted by the LHS hypothesis.

Estimating effective population size for a cestode parasite infecting three-spined sticklebacks.

Remarkably few attempts have been made to estimate contemporary effective population size (Ne) for parasitic species, despite the valuable perspectives it can offer on the tempo and pace of parasite evolution as well as coevolutionary dynamics of host-parasite interactions. In this study, we utilized multi-locus microsatellite data to derive single-sample and temporal estimates of contemporary Ne for a cestode parasite (Schistocephalus solidus) as well as three-spined stickleback hosts (Gasterosteus aculeatus) in lakes across Alaska. Consistent with prior studies, both approaches recovered small and highly variable estimates of parasite and host Ne. We also found that estimates of host Ne and parasite Ne were sensitive to assumptions about population genetic structure and connectivity. And, while prior work on the stickleback-cestode system indicates that physiographic factors external to stickleback hosts largely govern genetic variation in S. solidus, our findings indicate that stickleback host attributes and factors internal to the host - namely body length, genetic diversity and infection - shape contemporary Ne of cestode parasites.

The cestode parasite Schistocephalus pungitii: castrator or nutrient thief of ninespine stickleback fish?

In this investigation, the host-parasite relationship of ninespine stickleback fish Pungitius pungitius and the cestode parasite Schistocephalus pungitii was studied using samples from Dog Bone Lake, Kenai Peninsula, Alaska, to test the hypothesis that S. pungitii is a castrator of ninespine stickleback. Infected, adult females of all sizes (ages) were capable of producing clutches of eggs. S. pungitii had a negative effect on the ability of host females to produce a clutch, which was related to increasing parasite:host mass ratio (parasite index, PI). Among infected females with egg clutches, both clutch size and egg size were reduced; and the reduction increased with greater PI. The results of this study are consistent with the hypothesis that S. pungitii causes host sterility as a result of simple nutrient theft and is not a true castrator as hypothesized in earlier reports. The degree of parasite-induced sterility appears to vary among populations of the ninespine stickleback, perhaps reflecting differences in resource availability. Populations of ninespine stickleback appear to show a greater reduction in host reproductive capacity with PI than populations of the threespine stickleback infected by Schistocephalus solidus, possibly owing, in part, to the length-adjusted somatic mass of the threespine stickleback being greater.

Mutual dilution of infection by an introduced parasite in native and invasive stream fishes across Hawaii.

The presence of introduced hosts can increase or decrease infections of co-introduced parasites in native species of conservation concern. In this study, we compared parasite abundance, intensity, and prevalence between native Awaous stamineus and introduced poeciliid fishes by a co-introduced nematode parasite (Camallanus cotti) in 42 watersheds across the Hawaiian Islands. We found that parasite abundance, intensity and prevalence were greater in native than introduced hosts. Parasite abundance, intensity and prevalence within A. stamineus varied between years, which largely reflected a transient spike in infection in three remote watersheds on Molokai. At each site we measured host factors (length, density of native host, density of introduced host) and environmental factors (per cent agricultural and urban land use, water chemistry, watershed area and precipitation) hypothesized to influence C. cotti abundance, intensity and prevalence. Factors associated with parasitism differed between native and introduced hosts. Notably, parasitism of native hosts was higher in streams with lower water quality, whereas parasitism of introduced hosts was lower in streams with lower water quality. We also found that parasite burdens were lower in both native and introduced hosts when coincident. Evidence of a mutual dilution effect indicates that introduced hosts can ameliorate parasitism of native fishes by co-introduced parasites, which raises questions about the value of remediation actions, such as the removal of introduced hosts, in stemming the rise of infectious disease in species of conservation concern.

Fecundity compensation and fecundity reduction among populations of the three-spined stickleback infected by Schistocephalus solidus in Alaska.

We surveyed nine populations of the three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus from south-central Alaska for two apparent forms of tolerance to infection in females capable of producing egg clutches notwithstanding large parasite burdens. Seven populations exhibited fecundity reduction, whereas two populations showed fecundity compensation. Our data suggest that fecundity reduction, a side effect resulting from nutrient theft, occurs in two phases of host response influenced by the parasite : host body mass (BM) ratio. The first is significantly reduced ovum mass without significant reduction in clutch size, and the second one involves significant reductions in both ovum mass and clutch size. Thus, ovum mass of host females who are functionally being starved through nutrient theft seems to be more readily influenced by parasitism and, therefore, decreased before clutch size is reduced. This inference is consistent with expectations based on the biology of and effect of feeding ration on reproduction in stickleback females. Fecundity compensation appears to be uncommon among populations of three-spined stickleback in Alaska and rare among populations throughout the northern hemisphere. Fecundity reduction seems to be common, at least among stickleback populations in Alaska.

Freshwater Colonization, Adaptation, and Genomic Divergence in Threespine Stickleback.

The Threespine Stickleback is ancestrally a marine fish, but many marine populations breed in fresh water (i.e., are anadromous), facilitating their colonization of isolated freshwater habitats a few years after they form. Repeated adaptation to fresh water during at least 10 My and continuing today has led to Threespine Stickleback becoming a premier system to study rapid adaptation. Anadromous and freshwater stickleback breed in sympatry and may hybridize, resulting in introgression of freshwater-adaptive alleles into anadromous populations, where they are maintained at low frequencies as ancient standing genetic variation. Anadromous stickleback have accumulated hundreds of freshwater-adaptive alleles that are disbursed as few loci per marine individual and provide the basis for adaptation when they colonize fresh water. Recent whole-lake experiments in lakes around Cook Inlet, Alaska have revealed how astonishingly rapid and repeatable this process is, with the frequency of 40% of the identified freshwater-adaptive alleles increasing from negligible (∼1%) in the marine founder to ≥50% within ten generations in fresh water, and freshwater phenotypes evolving accordingly. These high rates of genomic and phenotypic evolution imply very intense directional selection on phenotypes of heterozygotes. Sexual recombination rapidly assembles freshwater-adaptive alleles that originated in different founders into multilocus freshwater haplotypes, and regions important for adaptation to freshwater have suppressed recombination that keeps advantageous alleles linked within large haploblocks. These large haploblocks are also older and appear to have accumulated linked advantageous mutations. The contemporary evolution of Threespine Stickleback has provided broadly applicable insights into the mechanisms that facilitate rapid adaptation.

Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution.

Similar forms often evolve repeatedly in nature, raising long-standing questions about the underlying mechanisms. Here, we use repeated evolution in stickleback to identify a large set of genomic loci that change recurrently during colonization of freshwater habitats by marine fish. The same loci used repeatedly in extant populations also show rapid allele frequency changes when new freshwater populations are experimentally established from marine ancestors. Marked genotypic and phenotypic changes arise within 5 years, facilitated by standing genetic variation and linkage between adaptive regions. Both the speed and location of changes can be predicted using empirical observations of recurrence in natural populations or fundamental genomic features like allelic age, recombination rates, density of divergent loci, and overlap with mapped traits. A composite model trained on these stickleback features can also predict the location of key evolutionary loci in Darwin's finches, suggesting that similar features are important for evolution across diverse taxa.

Morphological responses of a stream fish to water impoundment.

Water impoundment imposes fundamental changes on natural landscapes by transforming rivers into reservoirs. The dramatic shift in physical conditions accompanying the loss of flow creates novel ecological and evolutionary challenges for native species. In this study, we compared the body shape of Cyprinella venusta collected from eight pairs of river and reservoir sites across the Mobile River Basin (USA). Geometric morphometric analysis of the body shape showed that river populations differ from reservoir populations. Individuals inhabiting reservoirs are deep-bodied and have a smaller head, a more anterior dorsal fin, a shorter dorsal fin base and a more ventral position of the eye than C. venusta in streams. The direction of shape divergence within reservoir-river pairs was consistent among pairs of sites, and the shape of C. venusta in reservoirs is strongly correlated with reservoir size. These findings show that physical characteristics of reservoirs drive changes in the morphological attributes of native fish populations, indicating that water impoundment may be an important, yet largely unrecognized, evolutionary driver acting on aquatic biodiversity.