Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes

Abbreviations of the complex life cycle of trematodes, from three to two hosts, have occurred repeatedly and independently among trematode lineages. This is usually facultative and achieved via progenesis: following encystment in the second intermediate host, the metacercaria develops precociously into an egg-producing adult, bypassing the need to reach a definitive host. Given that it provides relatively cheap insurance against a shortage of definitive hosts, it is not clear why facultative progenesis has only evolved in a few taxa. Here a comparative approach is used to test whether progenetic trematodes are characterized by larger body size and egg volumes, two traits that correlate with other key life history features, than other trematodes. These traits may constrain the evolution of progenesis, because precocious maturation might be impossible when the size difference between the metacercaria and a reproductive adult is too large. First, trematode species belonging to genera in which progenesis has been documented were found not to differ significantly from other trematode species. Second, using within-genus paired comparisons across 19 genera in which progenesis has been reported, progenetic species did not differ, with respect to body size or egg size, from their non-progenetic congeners. Third, using intraspecific paired comparisons in species where progenesis is facultative, no difference was observed in the sizes of eggs produced by worms in both the intermediate and definitive host, suggesting that opting for progenesis does not influence the size of a worm's eggs. Overall, the lack of obvious differences in body or egg size between trematodes with truncated life cycles and those with the normal three-host cycle indicates that basic life history characteristics are not acting as constraints on the evolution of progenesis; trematodes of all sizes can do it. Why facultative progenesis is not more widespread remains a mystery.     

High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bethedging Strategy in the Face of Environmental Unpredictability

Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species(Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable(e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions(e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes.     

Effects of egg size on the development time of non-feeding larvae

The evolution of egg size in marine invertebrates remains a topic of central importance for life-history biologists, and the pioneering work of Vance has strongly influenced our current views. Vance's model and most models developed since have assumed that increases in egg size result in an increase in the prefeeding period of marine invertebrate larvae. For lecithotrophic species, this means that the entire development period should be correlated with egg size. Despite the importance of this assumption, it has not been tested at the appropriate scale-within species. We investigated the effects of egg size on development time for three lecithotrophic species from two phyla: the ascidians Phallusia obesa and Ciona intestinalis, and the echinoid Heliocidaris erythrogramma. We found that within individual broods of eggs, larger eggs took longer than smaller eggs to develop or become metamorphically competent larvae. It has long been recognized that producing larger eggs decreases fecundity, but our results show that increasing egg size also carries the extra cost of an extended planktonic period during which mortality can occur. The substantial variation in egg sizes observed within broods may represent a bet-hedging strategy by which offspring with variable dispersal potentials are produced.     

Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages

The transmission stages of parasites are key determinants of parasite fitness, but they also incur huge mortality. Yet the selective forces shaping the sizes of transmission stages remain poorly understood. We ran a comparative analysis of interspecific variation in the size of transmission stages among 404 species of parasitic trematodes. There are two transmission steps requiring infective stages in the life cycle of trematodes: transmission from the definitive to the first intermediate (snail) host is achieved by eggs and/or the miracidia hatched from those eggs, and transmission from the first to the second intermediate host is achieved by free-swimming cercariae. The sizes of these stages are under strong phylogenetic constraints. Our results show that taxonomy explains >50% of the unaccounted variance in linear mixed models, with most of the variance occurring at the superfamily level. The models also demonstrated that mollusc size is positively associated with egg volume, miracidial volume and cercarial body volume, but not with the relative size of the cercarial tail. In species where they encyst on substrates, cercariae have significantly larger bodies than in species penetrating chordates, although the relative size of the cercarial tail of species using chordates as second intermediate hosts was larger than in other trematode species. Habitat also matters, with larger cercarial tails seen in freshwater trematodes than in marine ones, and larger miracidial volumes in freshwater species than in marine ones. Finally, the latitude (proxy for local temperature) at which the trematode species were collected had no effect on the sizes of transmission stages. We propose that resource availability within the snail host, the probability of contacting a host, and the density and viscosity of the water medium combine to select for different transmission stage sizes.     

Ecological and environmental factors related to variation in egg size of New World flycatchers

Geographical variation in egg size is well documented for several taxa, but remains insufficiently described for birds in spite of a well‐known latitudinal gradient in clutch size. Several hypotheses have been proposed to explain avian egg size variation; however, they were not tested on a continental scale. Egg size is a key component of reproductive investment that influences offspring fitness. It is thought to vary geographically as one of a set of correlated life‐history traits that are under selection from varying ecological conditions. We completed a comprehensive literature review and calculated egg sizes for the most widespread clade within tyrant flycatchers, describing for the first time the geographical variation in egg size on a continental scale. We examined the relative support for ecological and environmental variables in explaining egg size variation using multi‐model inference and linear mixed models controlled for phylogenetic autocorrelation among species. We tested five hypotheses and found that: larger eggs occur in colder sites, which is consistent with the embryonic temperature hypothesis; medium/long‐distance migrants had smaller eggs than resident species while short‐distance migrants had the largest eggs; neither species clutch size, nor species nest type, nor evapotranspiration seasonality influenced egg size. Avian egg size is larger in Austral and Neotropical America (ANA), where species are resident or short‐distance migrants, and smaller across the medium/long‐distance migrants of the Nearctic region. In addition, while clutch size increases towards higher northern latitudes and is almost invariable across ANA species, egg sizes vary largely across ANA sites, increasing with southern latitudes and higher elevations and being influenced by summer temperature. While the embryonic temperature hypothesis has been usually linked to parental nest attentiveness, we highlight that environmental temperatures also have strong effects in shaping investment in egg size.     

Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

Information about transmission opportunities triggers a life-history switch in a parasite

Many microbial pathogens can switch to new hosts or adopt alternative transmission routes as environmental conditions change, displaying unexpected flexibility in their infection pathways and often causing emerging diseases. In contrast, parasitic worms that must develop through a fixed series of host species appear less likely to show phenotypic plasticity in their transmission pathways. Here, I demonstrate experimentally that a trematode parasite, Coitocaecum parvum, can accelerate its development and rapidly reach precocious maturity in its crustacean intermediate host in the absence of chemical cues emanating from its fish definitive host. Juvenile trematodes can also mature precociously when the mortality rate of their intermediate hosts is increased. Eggs produced by precocious adults hatch into viable larvae, capable of pursuing the parasite's life cycle. In the absence of chemical cues from fish hosts, the size of eggs released by precocious trematodes in their intermediate hosts becomes more variable, possibly indicating a bet-hedging strategy. These results illustrate that parasitic worms with complex life cycles have development and transmission strategies that are more plastic than commonly believed, allowing them to skip one host in their cycle when they perceive limited opportunities for transmission.     

香港淡水及海产贝类感染吸虫幼虫期的调查研究

作者于1983年4月及1986年4月二次在香港检查该地区20个村庄11种淡水螺(共11680粒),及14个海区包括红树林地带和无红树林的海滩中的22种海产贝类(共12580粒)。查获26种吸虫幼虫期,其中12种见于淡水螺(5种〕,8种寄生于红树林地带的海螺(7种),5种寄生于无红树林海区的贝类(6种),1种见于在红树林地带和无红树林海滩生存的海螺(5种)。寄生淡水螺的吸虫幼虫期分隶于Cortrematidae;Maseniidae;Schistosomatidae;Notocotylidae;Strigeidae;Paramphi-stomidae;Plagiorchidae;Philophthalmidaes;Microphallidae及Heterophyidae等科。寄生于海产贝类的吸虫幼虫期分隶于Philophthalmidae; Heterophyidae;Fellodistomidae; Cyathoco-tylidae;Echinostomatidae;Opecoelidae等科及Plagiorchioidea总科。     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Structure and temporal variation of trematode and gastropod communities in a freshwater ecosystem.

The infro- and component community dynamics of digenetic trematodes in a freshwater gastropod community were examined over a 33-month period. The gastropod and trematode communities were composed of 17 and 10 species respectively. A total of 9,831 snails was collected; among them, 192 belonging to 14 species were infected by larval trematodes. The size of infected snails was significantly greater than that of healthy ones, and the increase of prevalence with size/age was interpreted as related to the increased probability of ultimately becoming parasitized. The trematode community was rich in allogenic species, but the most frequent trematode (cercariaeum) was autogenic and generalist (a range of 12 snail host species). There was a significantly positive relationship between the frequency of trematode species in the community and the number of first intermediate host species. A great temporal heterogeneity occurred in the prevalence of the snails, mainly attributed to the great temporal fluctuations of snail host populations and the variability of freshwater ecological conditions. The data on the occurrence of larval trematodes in 14 host species over the 33-month study allowed indicate a significant negative correlation between the abundance of gastropods and the prevalence of trematodes.     

Life history and body size evolution in Holopedium gibberum Zaddach (Crustacea, Cladocera)

SUMMARY. 1. Body size, development, sheath size and relative egg size were examined in two populations of Holopedium gibberum Zaddach. The populations were chosen because of differences in juvenile versus adult mortality.
2. The population subject to food limitation and predation from icthyoplankton (high juvenile mortality) exhibited large size at birth and maturity, large sheath size, and eggs which were relatively large compared to the adult. In contrast, individuals in the population exposed to predation by golden shiner (high adult mortality) were smaller at birth and maturity, had a smaller sheath, and produced relatively small eggs.
3. I contrast body size and relative egg sizes of these H. gibberum populations with literature values for all Cladocera, and propose a general hypothesis for the evolution of relative egg size in Cladocera.     

Body-size effect on egg size in eublepharid geckos (Squamata: Eublepharidae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal

Within a single clutch, smaller species of ectotherms generally lay a smaller number of relatively larger eggs than do larger species. Many hypotheses explaining both the interspecific negative allometry in egg size and egg size–number trade-off postulate the existence of an upper limit to the egg size of larger species. Specifically, in lizards, large eggs of large species could have too long a duration of incubation, or they could be too large to pass through the pelvic opening, which is presumably constrained mechanically in larger species. Alternatively, negative allometry could be a result of limits affecting eggs of smaller species. Under the latter concept, hatchling size in smaller species may be close to the lower limit imposed by ecological interactions or physiological processes, and therefore smaller species have to invest in relatively larger offspring. Contrary to these lower limit hypotheses, explanations based on the existence of an upper limit always predict negative egg-size allometry even in animals with invariant clutch size, in which naturally there is no egg size–number trade-off. We studied egg-size allometry in lizards of the family Eublepharidae, a monophyletic group of primitive geckos with large variance in body size and an invariant number of two eggs per clutch. We found an isometric relationship between egg and female size that does not support the upper limit hypotheses.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 527–532.     

Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes

Measuring biodiversity is difficult. This has led to efforts to seek taxa whose species richness correlates with the species richness of other taxa. Such indicator taxa could then reduce the time and cost of assessing the biodiversity of the more extensive community. The search for species richness correlations has yielded mixed results, however. This may be primarily because of the lack of functional relationships between the taxa studied. Trematode parasites are highly promising bioindicators. Diverse assemblages of larval trematode parasites are easily sampled in intermediate host snails. Through their life cycles these parasites are functionally coupled with the surrounding free-living diversity of vertebrate and invertebrate animals. It has been shown that larval trematodes in snails correlate positively with bird diversity and abundance. Here, we explore whether trematodes also correlate with standard measures of fishes, and large and small benthos, for 32 sites in three wetlands. We found associations between trematodes and benthic communities that were not consistent across wetlands. The associations were, however, consistently positive for large benthic species richness and density. Some of the contrasting associations between trematode and benthos may be explained by negative associations between large and small benthos. We found no associations with fish communities (probably because of the inadequacy of standard “snapshot” sampling methods for highly mobile fishes). The results support further exploration of trematodes as bioindicators of diversity and abundance of animal communities. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Leaf litter transport and retention in a tropical Rift Valley stream: an experimental approach

The impact of a drought on freshwater snail and trematode communities was investigated in a lake. Before the drought, 15 gastropod species (Valvatidae, Planorbidae, Lymnaeidae, Ancylidae, Physidae) and 10 trematode species (cercariaeum, xiphidiocercariae, echinostome, furcocercariae, notocotyle, lophocercous) were recorded. The rate of parasitism was 5.13% and there were 11 host species. The 2 major consequences of desiccation were the disappearance of snails, except Valvata piscinalis and Lymnaea peregra, and the absence of trematodes infecting the surviving snails. As soon as favourable conditions were restored, the littoral area was recolonized, first by hygrophilic and amphibious species, second by aquatic species. Nine months after the drought, the gastropod community was restored. Recolonization by the trematodes was delayed compared with that of gastropods. During the study, the overall prevalence was equal to 0.36% and only 4 trematode species and 5 host species were recorded. Because of the great variability of freshwater ecosystems, long-term studies are necessary to understand the dynamics of snail and trematode populations and determine the regulatory effect of parasitism in the field.     

The role of female investment in a sexual arms race

Forced copulations are common among waterfowl species (Anatidae), a group with relatively large eggs and very precocial young. They can be viewed as the outcome of an overt sexual conflict, and an evolutionary arms race between the sexes. We examined the female choice hypothesis suggested, but not properly tested by Briskie and Montgomerie (1997) and Montgomerie and Briskie (2007), that penis size in male ducks might correlate with female investment in eggs, predicting that in species where females lay larger eggs, penis size might be larger, because females would be more reluctant to abandon their eggs if forced to copulate. A larger data set than in earlier studies enabled us to test that hypothesis in a comparative way. Our results compelled us to reject the female choice hypothesis since egg size is negatively correlated with penis length and the number of vaginal spirals, both being seen as adaptations to frequent forced copulations. The apparent trade-off between egg size and morphological defences (vaginal spirals) is strong particularly among monogamous species. Overall, we conclude that factors that set a lower limit for egg size constrain the morphological defences of females and the arms race between the sexes in waterfowl.     

SELF-FERTILIZATION VERSUS CROSS-FERTILIZATION IN THE HERMAPHRODITIC FRESHWATER SNAIL BULINUS GLOBOSUS

Self-fertilization depression of fitness in the freshwater hermaphroditic snail Bulinus globosus, an intermediate host of the parasitic trematode Schistosoma, has been studied in a strain originating from Niger. B. globosus is an outcrosser that can self-fertilize when isolated before any copulation has occurred. The self-fertilization depression has been estimated during two successive generations. In the first generation, selfing was compared to outcrossing. Within each mating system group, selfing and outcrossing were compared again in the second generation. A striking difference was shown in favor of cross-fertilization for the number of eggs laid, the survival at birth of young snails and the number of snails reaching sexual maturity. The overall self-fertilization depression is 0.920 after two generations of selfing. We discuss the relative role of selfing and outcrossing in the evolution of freshwater snail populations.     

Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish

1.?Maternal reproductive investment is thought to reflect a trade-off between offspring size and fecundity, and models generally predict that mothers inhabiting adverse environments will produce fewer, larger offspring. More recently, the importance of environmental unpredictability in influencing maternal investment has been considered, with some models predicting that mothers should adopt a diversified bet-hedging strategy whilst others a conservative bet-hedging strategy. 2.?We explore spatial egg size and fecundity patterns in the freshwater fish southern pygmy perch (Nannoperca australis) that inhabits a diversity of streams along gradients of environmental quality, variability and predictability. 3.?Contrary to some predictions, N.?australis populations inhabiting increasingly harsh streams produced more numerous and smaller eggs. Furthermore, within-female egg size variability increased as environments became more unpredictable. 4.?We argue that in harsh environments or those prone to physical disturbance, sources of mortality are size independent with offspring size having only a minor influence on offspring fitness. Instead, maternal fitness is maximized by producing many small eggs, increasing the likelihood that some offspring will disperse to permanent water. We also provide empirical support for diversified bet-hedging as an adaptive strategy when future environmental quality is uncertain and suggest egg size may be a more appropriate fitness measure in stable environments characterized by size-dependent fitness. These results likely reflect spatial patterns of adaptive plasticity and bet-hedging in response to both predictable and unpredictable environmental variance and highlight the importance of considering both trait averages and variance. 5.?Reproductive life-history traits can vary predictably along environmental gradients. Human activity, such as the hydrological modification of natural flow regimes, alters the form and magnitude of these gradients, and this can have both ecological and evolutionary implications for biota adapted to now non-existent natural environmental heterogeneity.     

Spatial and temporal variations in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts

The component community of larval trematodes infecting the mudsnail Hydrobia ventrosa (Montagu) was examined in coastal lagoons of the southern Baltic Sea among different host subpopulations in relation to the structure of the waterfowl community. The 10 trematode species observed represent the families Notocotylidae (1), Echinostomatidae (1 or 2), Heterophyidae (2). Monorchidae (1). Microphallidae (3 or 4), Psilostomatidae (1), and Hemiuridae (1). Eight of these species infect waterfowl as adults. The structure of the trematode communities was similar between sampling sites. Seven trematode taxa were commonly found at all sampling sites. Prevalence values of the 6 most abundant taxa, which infect birds as final hosts, were significantly different between neither sampling sites nor across year. Overall trematode prevalence in H. ventrosa fluctuated seasonally. Prevalence usually peaked in summer between July and September or October. Low prevalences were observed in late winter and early spring. In contrast, the seasonal maximum in waterfowl numbers differed between areas because of significant spatial differences in the bird community structure. The species composition of the component trematode community of H. ventrosa in the coastal lagoons of the southern Baltic Sea is more or less independent of the species composition of the waterfowl community. This independence presumably results from the lack of host specificity in most of the observed trematode species. Otherwise, the low host specificity in combination with the enormous waterfowl diversity in the coastal lagoons might explain the stability of the prevalence pattern of the component trematode community.     

Neorickettsia risticii is vertically transmitted in the trematode Acanthatrium oregonense and horizontally transmitted to bats

Potomac horse fever is known to be transmitted through the ingestion of caddisflies parasitized with Neorickettsia (formerly Ehrlichia) risticii-infected metacercaria. However, the species of trematode involved and how N. risticii is maintained in nature are unknown. In this study, gravid trematodes were recovered from the intestines of 12 out of 15 Eptesicus fuscus big brown bats and eight out of nine Myotis lucifugus little brown bats from various sites in Pennsylvania, USA. Trematode specimens isolated from six E. fuscus bats contained N. risticii DNA. The trematode was identified as Acanthatrium oregonense. N. risticii was detected within individual trematode eggs by polymerase chain reaction as well as by immunofluorescence labelling with an anti-N. risticii antibody, indicating that N. risticii is vertically transmitted (from adult to egg) in A. oregonense. Furthermore, N. risticii DNA was detected in the blood, liver or spleen of 23 out of 53 E. fuscus and M. lucifugus bats, suggesting that N. risticii can also be transmitted horizontally from trematode to bat. These results indicate that A. oregonense is a natural reservoir and probably a vector of N. risticii.     

Egg-size evolution in aquatic environments: does oxygen availability constrain size?

Selection against large eggs has been proposed for aquatic environments, putatively because large eggs should have more difficulty obtaining the required oxygen. Here, we use brown trout (Salmo trutta) eggs to provide an experimental test of this hypothesis. At high levels of dissolved oxygen (14 mg l(-1)), egg survival was high and independent of egg size. At low oxygen levels (2.3 mg l(-1)), survival decreased overall, and was higher for large-egged than small-egged siblings. Thus, contrary to conventional expectation, low oxygen levels selected for large rather than small eggs. A second experiment using Atlantic salmon (S. salar) eggs indicated that oxygen consumption increases relatively slowly with increasing egg mass (allometric constant = 0.44). The failure of the conventional 'bigger is worse during incubation' hypothesis may thus be due to the erroneous assumption that oxygen consumption increases at a greater rate with increasing egg mass than does the egg surface area that is available for oxygen diffusion. We also demonstrate, using data from Atlantic salmon, that nest-specific oxygen consumption decreases with increasing egg size, but that this effect is more pronounced for large than for small females. This may help to explain the positive correlation between adult body size and egg size observed in fishes that cluster their eggs.