Géraldine Loot

Species-specific responses to landscape fragmentation: implications for management strategies

Habitat fragmentation affects the integrity of many species, but little is known about species‐specific sensitivity to fragmentation. Here, we compared the genetic structure of four freshwater fish species differing in their body size (Leuciscus cephalus; Leuciscus leuciscus; Gobio gobio and Phoxinus phoxinus) between a fragmented and a continuous landscape. We tested if, overall, fragmentation affected the genetic structure of these fish species, and if these species differed in their sensitivity to fragmentation. Fragmentation negatively affected the genetic structure of these species. Indeed, irrespective of the species identity, allelic richness and heterozygosity were lower, and population divergence was higher in the fragmented than in the continuous landscape. This response to fragmentation was highly species‐specific, with the smallest fish species (P. phoxinus) being slightly affected by fragmentation. On the contrary, fish species of intermediate body size (L. leuciscus and G. gobio) were highly affected, whereas the largest fish species (L. cephalus) was intermediately affected by fragmentation. We discuss the relative role of dispersal ability and effective population size on the responses to fragmentation we report here. The weirs studied here are of considerable historical importance. We therefore conclude that restoration programmes will need to consider both this societal context and the biological characteristics of the species sharing this ecosystem.

Geography and host specificity: Two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae)

Parasite species with global distributions and complex life cycles offer a rare opportunity to study alternative mechanisms of speciation and evolution in a single model. Here, genealogy and genetic structure, with respect to geography and fish host preference, have been analyzed for Ligula intestinalis, a tapeworm affecting freshwater fish. The data analyzed consisted of 109 tapeworms sampled from 13 fish host species in 18 different localities on a macrogeographic scale. Two mitochondrial genes, cytochrome oxidase subunit I and cytochrome B, and the nuclear sequence of intergenic transcribed spacer 2 (ITS2) were used for the genetic reconstruction. Different evolutionary patterns were found at the local and at the global geographic scales. On a local scale, the flat genetic structure was mainly attributed to contiguous range expansion. Migrating birds are the most likely cause of the homogenisation of the whole population, preventing the creation of significant genetic barriers. By contrast, on a global scale, genetically distant and well-separated clusters are present in different geographic areas. Reproductive isolation was found even between clades living in sympatry and infecting the same definitive host, suggesting the existence of efficient biologically determined genetic barriers, and thus possibly separate species. Although the ITS2 sequences were found to display considerable intragenomic variability, their relationships were generally in good agreement with the topology derived from mitochondrial genes.

Evidence for host variation in parasite tolerance in a wild fish population

Hosts can protect themselves against parasites by actively reducing parasites burden (i.e. resistance) or by limiting the damages caused by parasites (i.e. tolerance). Disentangling between tolerance and resistance is important for predicting the evolutionary outcomes of host-parasite interaction. Dace (Leuciscus leuciscus) are often parasitized by the ectoparasite Tracheliastes polycolpus which feeds on (and destroys) fins, reducing thus the host’s condition. We tested the hypothesis that genetically-based variation in ectoparasite tolerance exists in a wild dace population. We found that moderately heterozygous dace, which are less resistant than highly heterozygous or homozygous dace, tolerated better the effect imposed by T. polycolpus for a given parasite burden. However, tolerance also varied upon environmental conditions, suggesting that genetic and environmentally-based variation exists for both resistance and tolerance in this natural host-parasite system. Moreover, a negative genetic correlation may exist between tolerance and resistance, and hence several evolutionary outcomes are possible in this interacting system.

Why do parasitized hosts look different? Resolving the "chicken-egg" dilemma.

Phenotypic differences between infected and non-infected hosts are often assumed to be the consequence of parasite infection. However, pre-existing differences in hosts’ phenotypes may promote differential susceptibility to infection. The phenotypic variability observed within the host population may therefore be a cause rather than a consequence of infection. In this study, we aimed at disentangling the causes and the consequences of parasite infection by calculating the value of a phenotypic trait (i.e., the growth rate) of the hosts both before and after infection occurred. That procedure was applied to two natural systems of host–parasite interactions. In the first system, the infection level of an ectoparasite (Tracheliastes polycolpus) decreases the growth rate of its fish host (the rostrum dace, Leuciscus leuciscus). Reciprocally, this same phenotypic trait before infection modulated the future level of host sensitivity to the direct pathogenic effect of the parasite, namely the level of fin degradation. In the second model, causes and consequences linked the growth rate of the fish host (the rainbow smelt, Osmerus mordax) and the level of endoparasite infection (Proteocephalus tetrastomus). Indeed, the host’s growth rate before infection determined the number of parasites later in life, and the parasite biovolume then decreased the host’s growth rate of heavily infected hosts. We demonstrated that reciprocal effects between host phenotypes and parasite infection can occur simultaneously in the wild, and that the observed variation in the host phenotype population was not necessarily a consequence of parasite infection. Disentangling the causality of host–parasite interactions should contribute substantially to evaluating the role of parasites in ecological and evolutionary processes.

Evidence of parasite‐mediated disruptive selection on genetic diversity in a wild fish population

Identifying the processes maintaining genetic variability in wild populations is a major concern in conservation and evolutionary biology. Parasite‐mediated selection may strongly affect genetic variability in wild populations. The inbreeding depression theory predicts that directional selection imposed by parasites should act against the most inbred hosts, thus favouring genetic diversity in wild populations. We have tested this prediction by evaluating the strength and shape of the relationship between the load of a harmful fin‐feeder ectoparasite (Tracheliastes polycolpus) and the genome‐wide genetic diversity (i.e. heterozygosity measured at a set of 15 microsatellites) of its fish host, the rostrum dace (Leuciscus leuciscus). Contrary to expectation, we found a nonlinear relationship between host genetic diversity and ectoparasite load, with hosts that were either homozygous or heterozygous harbouring significantly fewer parasites than hosts with an intermediate level of heterozygosity. This relationship suggests that parasites could increase the variance of global heterozygosity in this host population through disruptive selection on genetic diversity. Moreover, when genetic diversity was measured at each locus separately, we found two very strong positive associations between host genetic diversity and the ectoparasite load. This latter result has three main implications: (i) genome‐wide effect cannot alone explain the nonlinear relationship between global heterozygosity and ectoparasite load, (ii) negative non‐additive allelic interactions (i.e. underdominance) may be a mechanism for resisting ectoparasite infection, and (iii) ectoparasites may favour homozygosity at some loci in this host population.

The disruption of dominance hierarchies by a non-native species: an individual-based analysis

We studied the effects of the exotic rainbow trout (Oncorhynchus mykiss) on the performance and the dominance hierarchy of native Atlantic salmon (Salmo salar) at the group and individual level using laboratory and semi-natural experiments. At the group level, we compared the effects of interspecific and intraspecific competition (substitutive and additive design) on behavioural responses and growth of young-of-the-year Atlantic salmon. At the individual level, the same design was used to evaluate: (1) the temporal consistency of behavioural responses, dominance hierarchy and growth rate of Atlantic salmon; (2) the pattern of correlations between behaviours; and (3) the relationship between individual growth rate and behaviour. In the laboratory, group-level analyses revealed a weak but similar effect of rainbow trout and intraspecific competition on the behaviour and growth of Atlantic salmon. In contrast, individual-based analyses demonstrated that rainbow trout (but not intraspecific competition) strongly affected behavioural strategy, dominance hierarchy and growth trajectory of individual Atlantic salmon. Specifically, behaviours, dominance status and growth rate of salmon were temporally consistent in the intraspecific environment, while these patterns were disrupted when rainbow trout were present. Similarly, we found that rainbow trout strongly affected behavioural correlations and the relationships between individual growth rate and behaviour. The semi-natural experiments confirmed these results as interspecific competition affected relationships between individual growth rate of salmon, initial weight and activity index. Overall, individual-based analyses highlighted important mechanisms that were concealed at the group level, and that may be crucial to understand ecological and evolutionary consequences of exotic species. Moreover, these results demonstrated that competition with an exotic species disrupts the hierarchical relationship among native individuals and may therefore represent a potential for a shift in selective pressure.

Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis

1. Understanding the ecological factors driving the burden and pathogenicity of parasites is challenging. Indeed, the dynamics of host-parasite interactions is driven by factors organized across nested hierarchical levels (e.g. hosts, localities), and indirect effects are expected owing to interactions between levels. 2. In this study, we combined Bayesian multilevel models, path analyses and a model selection procedure to account for these complexities and to decipher the relative effects of host- and environment-related factors on the burden and the pathogenicity of an ectoparasite (Tracheliastes polycolpus) on its fish host (Leuciscus leuciscus). We also tested the year-to-year consistency of the relationships linking these factors to the burden and the pathogenic effects of T. polycolpus. 3. We found significant relationships between the parasite burden and host-related factors: body length and age were positively related to parasite burden and heterozygous hosts displayed a higher parasite burden. In contrast, both host- and environment-related factors were linked to pathogenic effects. Pathogenicity was correlated negatively with host body length and positively with age; this illustrates that some factors (e.g. body length) showed inverse relationships with parasite burden and pathogenicity. Pathogenic effects were stronger in cooler upstream sites and where host density was lower. Path analyses revealed that these relationships between environment-related factors and pathogenic effects were direct and were not indirect relationships mediated by the host characteristics. Finally, we found that the strength and the shape of certain relationships were consistent across years, while they were clearly not for some others. 4. Our study illustrates that considering conjointly causal relationships among factors and the hierarchical structure of host-parasite interactions is appropriate for dissecting the complex links between hosts, parasites and their common environment.

PHENOTYPIC MODIFICATION OF ROACH (RUTILUS RUTILUS L.) INFECTED WITH LIGULA INTESTINALIS L. (CESTODA: PSEUDOPHYLLIDEA)

In European freshwater, cyprinid fish may be heavily infected by plerocercoids of the pseudophyllidea cestode Ligula intestinalis (L.). During their development, these parasites grow rapidly to a large size in the fishs body cavity, characteristically distending the abdomen. In this study, the influence of this tapeworm on roach (Rutilus rutilus L.) morphology was analyzed. Forty-five infected and 45 uninfected roach were collected from the Lavernose-Lacasse gravel pit in Toulouse, south western France and examined for 40 morphological measurements to study phenotypic modification of the body and 14 bilateral characters for an analysis of asymmetry. Results indicate that the degree of bilateral asymmetry does not change between infected and uninfected roach, despite the strong host-morphological modifications such as deformation of the abdomen, fin displacements at the level of the tail, and sagging of the vertebral column. The intensity of abdominal distension and fish morphology changes depends on the total parasite biomass present. Differences were observed in morphology at different levels of infection, which relate to established effects of L. intestinalis on the physiology and behavior of intermediate hosts. These morphological changes induced by the parasite could increase trophic transmission to the definitive avian hosts.

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.

The effects of abiotic factors and intraspecific versus interspecific competition on the diel activity patterns of Atlantic salmon (Salmo salar) fry

We conducted semi-natural experiments to measure the relative contribution of various environmental factors and intraspecific and interspecific competition with an exotic invader on the daytime and crepuscular activity levels of Atlantic salmon (Salmo salar) fry. We demonstrated that interspecific competition with the exotic rainbow trout (Oncorhynchus mykiss) significantly increases the daytime activity of Atlantic salmon. The effect of intraspecific competition on the daytime activity of salmon was half that of interspecific competition. This indicates that the effect of rainbow trout was a combination of increasing density and the identity of the competitor. We also demonstrated that the effect of rainbow trout was probably the result of territorial interference between species. Moreover, we showed that water temperature simultaneously played an important role in explaining daytime activity of Atlantic salmon. During twilight, we observed no effect of competition on salmon activity, but environmental c...