Evolutionary consequence of a change in life cycle complexity: A link between precocious development and evolution toward female‐biased sex allocation in a hermaphroditic parasite

The evolutionary consequences of changes in the complex life cycles of parasites are not limited to the traits that directly affect transmission. For instance, mating systems that are altered due to precocious sexual maturation in what is typically regarded as an intermediate host may impact opportunities for outcrossing. In turn, reproductive traits may evolve to optimize sex allocation. Here, we test the hypothesis that sex allocation evolved toward a more female‐biased function in populations of the hermaphroditic digenean trematode Alloglossidium progeneticum that can precociously reproduce in their second hosts. In these precocious populations, parasites are forced to self‐fertilize as they remain encysted in their second hosts. In contrast, parasites in obligate three‐host populations have more opportunities to outcross in their third host. We found strong support that in populations with precocious development, allocation to male resources was greatly reduced. We also identified a potential phenotypically plastic response in a body size sex allocation relationship that may be driven by the competition for mates. These results emphasize how changes in life cycle patterns that alter mating systems can impact the evolution of reproductive traits in parasites.     

Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea.

An important component of the parasite fauna of seabirds in arctic regions are the flukes (Digena). Different species of digeneans have life cycles which may consist of 1 intermediate host and no free-living larval stages, 2 intermediate hosts and 1 free-living stage, or 2 intermediate hosts and 2 free-living larval stages. This study examined the distribution of such parasites in the intertidal zones of the southern coast of the Barents Sea (northwestern Russia and northern Norway) by investigating 2 species of periwinkles (Littorina saxatilis and L. obtusata) which are intermediate hosts of many species of digeneans. A total of 26,020 snails from 134 sampling stations were collected. The study area was divided into 5 regions, and the number of species, frequency of occurrence and prevalence of different digenean species and groups of species (depending on life cycle complexity) were compared among these regions, statistically controlling for environmental exposure. We found 14 species of digeneans, of which 13 have marine birds as final hosts. The number of species per sampling station increased westwards, and was higher on the Norwegian coast than on the Russian coast. The frequency of occurrence of digeneans with more than 1 intermediate host increased westwards, making up a larger proportion of the digeneans among infected snails. This was significant in L. saxatilis. The prevalence of different species showed the same pattern, and significantly more snails of both species were infected with digeneans with complicated life cycles in the western regions. In L. saxatilis, environmental exposure had a statistically significant effect on the distribution of the most common digenean species. This was less obvious in L. obtusata. The causes of changing species composition between regions are probably (1) the harsh climate in the eastern part of the study area reducing the probability of successful transmission of digeneans with complicated life cycles, and (2) the distribution of different final hosts.     

Life cycles, molecular phylogeny and historical biogeography of the 'pygmaeus' microphallids (Digenea: Microphallidae): widespread parasites of marine and coastal birds in the Holarctic

SUMMARY The 'pygmaeus' microphallids (MPG) are a closely related group of 6 digenean (Platyhelminthes: Trematoda) Microphallus species that share a derived 2-host life cycle in which metacercariae develop inside daughter sporocysts in the intermediate host (intertidal and subtidal gastropods, mostly of the genus Littorina) and are infective to marine birds (ducks, gulls and waders). Here we investigate MPG transmission patterns in coastal ecosystems and their diversification with respect to historical events, host switching and host-parasite co-evolution. Species phylogenies and phylogeographical reconstructions are estimated on the basis of 28S, ITS1 and ITS2 rDNA data and we use a combination of analyses to test the robustness and stability of the results, and the likelihood of alternative biogeographical scenarios. Results demonstrate that speciation within the MPG was not associated with co-speciation with either the first intermediate or final hosts, but rather by host-switching events coincident with glacial cycles in the Northern Hemisphere during the late Pliocene/Pleistocene. These resulted in the expansion of Pacific biota into the Arctic-North Atlantic and periodic isolation of Atlantic and Pacific populations. Thus we hypothesize that contemporary species of MPG and their host associations resulted from fragmentation of populations in regional refugia during stadials, and their subsequent range expansion from refugial centres during interstadials.     

Imprecise naming: the anadromous and the sea spawning threespine stickleback should be discriminated by names

Two ecological forms of the threespine stickleback Gasterosteus aculeatus – a strictly marine form and an anadromous form – are often merged in the literature as a single “marine” form. Because we know virtually nothing of the life style of the two oceanic ecotypes in the sea and consequently nothing on reproductive isolation and gene flow I argue for a precise use of the ecological terms “marine” and “anadromous” for these two ecotypes. These terms should be self-describing. The frequent use of terms incorrectly describing intraspecific variation and life style of ecotypes can bias studies on community composition and interactions of populations.     

The parasitic dinoflagellates of marine crustaceans

Parasitic dinoflagellates have recently emerged as significant disease agents of commercially important crustaceans. For example, epizootics of Hematodinium have seriously affected certain crab and lobster fisheries. The parasitic dinoflagellates of crustaceans are, however, relatively unknown. Marine crustaceans are parasitized by two orders of dinoflagellates: the Blastodinida and the Syndinida. Crustaceans are also parasitized by the Paradinida and the Ellobiopsidae, taxa that have close historical ties and possible taxonomic affinities with the dinoflagellates. The taxonomy and life history patterns of the different parasitic species are largely dictated by their host-parasite relationships. For example, sporulation in the blastodinids occurs internally but is completed externally with the expulsion of spores via the anus of the host. The egg-parasitic chytriodinids sporulate externally after destroying their host egg. The tissue-dwelling syndinids have plasmodia that sporulate internally and generally kill their hosts upon the expulsion of the dinospores. Unfortunately, complete life cycles have not been elucidated for any of the parasitic forms, hence characteristics of the life cycles must be applied cautiously to the systematics of the taxa. For example, gamogony and the presence of resting cysts are only known from a few species; they probably occur in most species. Further work on the life cycles of the parasitic dinoflagellates of crustaceans should concentrate on establishing the life cycles of representative species from each order or family. Parasitic dinoflagellates infect copepods, amphipods, mysids, euphausiids, and decapods. Their pathogenicity varies with their invasiveness in the host. The gut-dwelling blastodinids are relatively benign, while the chytriodinids kill their host egg. Members of the pervasive Syndinida and Paradinida are overtly pathogenic and insidiously ramify throughout the hemal sinuses and organs of their hosts. Members of the Ellobiopsidae vary from the commensal Ellobiocystis to the overtly parasitic Thalassomyces. Host castration and feminization are common pathologic results of infection by these parasites. The severity of the castration is dependent upon the invasiveness of the parasitic species and the duration of the infection, while the degree of feminization is related to the stage at which the host acquires the infection. Most of the parasitic dinoflagellates occur in epizootics in their host populations. Recent epizootics of Hematodinium spp. have had severe effects on crustacean fisheries in Alaska, Virginia, and Scotland, and may potentially result in changes to the benthic communities of the hosts. The epizootics are often associated with host-parasite systems that occur in regions with unique hydrological features, such as fjords or poorly draining estuaries with shallow sills. These regions are ideal for the application of a “landscape” ecology approach that could lead to a better understanding of the epizootiology of parasitic dinoflagellates and other marine pathogens.     

Factors affecting trematode infection rates in freshwater mussels

Mussels are intermediate hosts of digenean trematodes, but determinants of these infections remain unknown. To address this problem, we collected duck mussels Anodonta anatina in eighteen lakes from northeastern Poland and examined how mussel age, sex, and the encrustation with zebra mussels Dreissena polymorpha and environmental conditions in lakes influenced infection rates. We also assessed parasitic preferences to host gonads and hepatopancreas and the impact of parasites on female fertility. Mussels were infected with Rhipidocotyle campanula and Phyllodistomum sp. Infection rates were higher in older and female mussels but were unrelated to the biomass of encrusting D. polymorpha and the trophy, thermal conditions, and Ca²⁺ availability. Parasites occupied gonads more often than hepatopancreas. Infected females were less likely to carry glochidia and incubated fewer glochidia. We suggest that the risk of infection by digenean trematodes increases with the amount of water processed by filter-feeding hosts and/or that parasites actively seek hosts which can provide them with abundant resources. This mechanism explains why parasites more often occupied older and female mussels and targeted their gonads. Future research on trematode-mussel interactions should integrate knowledge on different elements of the complex trematode life cycles, including effects of higher-order hosts such as fish.     

Increased abundance of snails and trematode parasites of <Emphasis Type="Italic">Fundulus heteroclitus</Emphasis> (L.) in restored New Jersey wetlands

The Hackensack Meadowlands District is a large heavily degraded, brackish marsh system in the urbanized northeastern region of New Jersey, USA. Six study sites were used, three of which were restored (Mill Creek, Skeetkill Creek and Vince Lombardi), and three others were unrestored (Richard DeKorte Park, Cedar Creek and Kingsland Creek). Highly significant differences were found with respect to snail abundance and gill parasite abundance. In the three restored sites, significantly more Littoridinops tenuipes were found, and Fundulus heteroclitus had significantly more digenean trematode metacercariae gill infections than at unrestored sites. As habitat quality improves following restoration, the number of suitable digenean trematode parasite hosts multiplies as substrate for benthic invertebrates (first intermediate host) increases and usage by other species, such as Fundulus spp. (second intermediate host), is encouraged, which then attracts more wading birds (definitive host). Though the restoration process enhances trophic complexity, including primary consumers (gastropods), secondary consumers (fish) and tertiary consumers (wading birds), and ultimately parasite diversity, restoration also helps facilitate parasite life cycles.     

Does a facultative precocious life cycle predispose the marine trematode Proctoeces cf. lintoni to inbreeding and genetic differentiation among host species?

Intraspecific variability in parasite life cycle complexity (number of hosts and species of hosts in the life cycle) may have an impact how parasite genetic variation is partitioned among individual parasites, host individuals or host species within a given area. Among digenean trematodes, a three-host life cycle is common. However, a few species are precocious and may reach sexual maturity in what is typically regarded as the second intermediate host. The objective of this study was to determine whether a precocious life cycle predisposes digeneans to possible inbreeding or genetic subdivision among host species. As a study system, we used the digenean Proctoeces cf. lintoni whose metacercariae precociously mature (facultative) without a cyst wall in the gonads of multiple sympatric species of keyhole limpets (Fissurella spp.), typically regarded as the second intermediate hosts. Genotyped parasites were collected from four species of limpets and the clingfish Sicyases sanguineus, the third and final host where sexual maturity occurs. We found very high microsatellite diversity, Hardy–Weinberg equilibrium over all genotyped individuals, and little to no genetic structuring among parasites collected from the different host species. The fact that metacercariae do not encyst in the keyhole limpets, coupled with the high mixing potential of an aquatic environment, likely promote panmixia in local populations of P. cf. lintoni.     

Tropics,trophics and taxonomy: the determinants of parasite‐associated host mortality

Empirical studies often reveal deleterious effects of parasites on host survival, but the ecological and environmental processes modulating parasite‐associated host mortality are not well understood. We conducted meta‐analysis of experimental studies assessing parasite‐associated mortality (n = 52) to evaluate broad‐scale patterns in host mortality risk relative to host or parasite taxon, parasite life cycle, or local environmental conditions. Overall, likelihood of host mortality was ～2.6 times higher among infected individuals when compared with hosts that either lacked parasites or had experimentally‐reduced parasite burdens. Parasites with complex life cycles reliant on predation‐mediated transmission generally were associated with higher mortality risk than those exploiting other transmission strategies. We also detected a negative relationship between parasite‐associated host mortality and latitude; host mortality risk declined by ～2.6% with each degree increase in latitude. This result indicated the likely importance of abiotic factors in determining parasite effects. Host taxonomy further influenced parasite‐associated mortality risk, with amphibian, fish, and mollusc hosts generally having higher hazard than arthropod, mammal, and bird hosts. Our results suggest patterns that conform to the predicted link between host mortality and parasite transmissibility, and pathogenicity. The relationship between host mortality and latitude in particular may portend marked shifts in host–parasite relationships pursuant to ongoing and projected global climate change.     

WIDESPREAD HOST‐DEPENDENT HYBRID UNFITNESS IN THE PEA APHID SPECIES COMPLEX

Linking adaptive divergence to hybrid unfitness is necessary to understand the ecological factors contributing to reproductive isolation and speciation. To date, this link has been demonstrated in few model systems, most of which encompass ecotypes that occupy relatively early stages in the speciation process. Here we extend these studies by assessing how host‐plant adaptation conditions hybrid fitness in the pea aphid, Acyrthosiphon pisum. We made crosses between and within five pea aphid biotypes adapted to different host plants and representing various stages of divergence within the complex. Performance of F1 hybrids and nonhybrids was assessed on a “universal” host that is favorable to all pea aphid biotypes in laboratory conditions. Although hybrids performed equally well as nonhybrids on the universal host, their performance was much lower than nonhybrids on the natural hosts of their parental populations. Hence, hybrids, rather than being intrinsically deficient, are maladapted to their parents’ hosts. Interestingly, the impact of this maladaptation was stronger in certain hybrids from crosses involving the most divergent biotype, suggesting that host‐dependent postzygotic isolation has continued to evolve late in divergence. Even though host‐independent deficiencies are not excluded, hybrid maladaptation to parental hosts supports the hypothesis of ecological speciation in this complex.     

Phylogenetic inference from platyhelminth life-cycle stages

Studies of the life cycle stages of digeneans and oncophoreans (= monogeneans and cestodes) indicate that these two groups had separate origins from free-living rhabdocoel-like ancestors and that the original single-host life cycles became 2-host cycles through accidental ingestion, in digeneans by free-swimming adults being ingested by vertebrates, and in cestodes by eggs being ingested by invertebrates. In both lines a third host was incorporated as a means of increasing the efficiency of transfer between hosts, in digeneans between the primary mollusc and the secondary vertebrate, and in cestodes between the secondary (“first intermediate”) host and the primary vertebrate host.     

Hitch-hiking parasite: a dark horse may be the real rider

Many parasites engaged in complex life cycles manipulate their hosts in a way that facilitates transmission between hosts. Recently, a new category of parasites (hitch-hikers) has been identified that seem to exploit the manipulating effort of other parasites with similar life cycle by preferentially infecting hosts already manipulated. Thomas et al. (Evolution 51 (1997) 1316) showed that the digenean trematodes Microphallus papillorobustus (the manipulator) and Maritrema subdolum (the hitch-hiker) were positively associated in field samples of gammarid amphipods (the intermediate host), and that the behaviour of Maritrema subdolum rendered it more likely to infect manipulated amphipods than those uninfected by M. papillorobustus. Here I provide experimental evidence demonstrating that M. subdolum is unlikely to be a hitch-hiker in the mentioned system, whereas the lucky candidate rather is the closely related but little known species, Microphallidae sp. no. 15 (Parassitologia 22 (1980) 1). As opposed to the latter species, Maritrema subdolum does not express the appropriate cercarial behaviour for hitch-hiking.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Life cycles shape parasite evolution: comparative population genetics of salmon trematodes

Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.     

Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons

Attention is drawn to the effects of parasites on their hosts, taking as a model the digenean parasites of teleosts (hereafter: fish) from lagoons along the French Mediterranean coast. Because digeneans have a heteroxenic life cycle, their impact is not limited to the definitive host, which harbours the sexual adults, but is extended to the first host (mollusc) and to the second host ("invertebrate" or fish). Adult parasites, in order to ensure efficient sexual reproduction, never cause excessive damage to their definitive host, usually only exploiting the intestinal fluids; however, the host must intensify its search for prey, which results in a diminished fitness. Within the first host, 'larval' stages of digenean parasites invade the gonads, resulting in its castration, then exhaustion and eventually death. The diversion of energy from the second hosts towards the parasites forces them to intensify their search for food, resulting in decreased fitness and an increased risk of being eaten; in addition, manipulation of the host's behaviour by parasites drives this host into the food chain of the definitive host. In lagoons, many individuals of almost all species of fish and invertebrates act as first, second and/or definitive hosts for digeneans. Obviously, parasites have a severe impact on the population dynamics of key taxa, on the food web and therefore also on the functioning of the whole lagoon ecosystem. Yet this impact has been largely overlooked or underestimated in functioning models, by ecologists, who tend to prioritize more apparent trophic relationships.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

From host–parasite systems to parasitic systems: Interactions of littoral mollusks of the genus <Emphasis Type="Italic">Littorina</Emphasis> with their trematode parasites

The idea of parasitic systems, formulated by V.N. Beklemishev 70 years ago, represents a conceptual tool for the analysis of populational and biocoenotic roles of parasites. The questions concerning longterm stable persistence of host–parasite systems in communities can be discussed meaningfully only within this concept. Importantly, the set of terms elaborated within the parasitic system concept is applicable not only to parasitology, but also contributes to the general knowledge of life cycles of organisms and differences in the environment. This concept provides an opportunity for comprehensive analysis of systems, based on any type of stable biocoenotic interactions in the community (predation, commensalism, competition, etc.). Trematode-based parasitic systems, involving populations of intertidal mollusks of the genus Littorina, allow demonstrating how the strong “negative” effect of parasites on hosts at the individual level (complete parasitic castration) can be compensated at the population level. Such compensation functions as a prerequisite for maintaining long-term stable interactions between populations of parasites and their hosts within parasitic system (the ecosystem, biocoenotic level).     

Microbial Diversity in the Eukaryotic SAR Clade: Illuminating the Darkness Between Morphology and Molecular Data

Despite their diversity and ecological importance, many areas of the SAR—Stramenopila, Alveolata, and Rhizaria—clade are poorly understood as the majority (90%) of SAR species lack molecular data and only 5% of species are from well‐sampled families. Here, we review and summarize the state of knowledge about the three major clades of SAR, describing the diversity within each clade and identifying synapomorphies when possible. We also assess the “dark area” of SAR: the morphologically described species that are missing molecular data. The majority of molecular data for SAR lineages are characterized from marine samples and vertebrate hosts, highlighting the need for additional research effort in areas such as freshwater and terrestrial habitats and “non‐vertebrate” hosts. We also describe the paucity of data on the biogeography of SAR species, and point to opportunities to illuminate diversity in this major eukaryotic clade. See also the video abstract here: https://youtu.be/_VUXqaX19Rw .     

Developmental plasticity in schistosomes and other helminths

Developmental plasticity in helminth life cycles serves, in most cases, to increase the probability of transmission between hosts, suggesting that the necessity to achieve transmission is a prominent selective pressure in the evolution of this phenomenon. Some evidence suggests that digenean trematodes from the genus Schistosoma are also capable of limited developmental responses to host factors. Here we review the currently available data on this phenomenon and attempt to draw comparisons with similar processes in the life cycles of other helminths. At present the biological significance of developmental responses by schistosomes under laboratory conditions remains unclear. Further work is needed to determine whether developmental plasticity plays any role in increasing the probability of schistosome transmission and life cycle propagation under adverse conditions, as it does in other helminth life cycles.