Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Scale‐invariance of niche breadth in fleas parasitic on small mammals

The resource specialization or niche breadth of a species is not fixed across populations, but instead varies over geographical space. A species may be a local specialist but a regional generalist, if it uses locally few resources that are substitutable across locations. In contrast, a species is a local generalist and a regional specialist if it uses locally many resources that cannot be substituted from 1 location to the next. Scale‐dependence can thus be a major factor in estimation of niche breadth. Here, we test for relationships between local and global estimates of host specificity (a measure of niche breadth for parasites) in fleas (Siphonaptera) parasitic on small mammals from 49 different regions within the Holarctic. Across all fleas, we found a strong, positive relationship between the number of host species that a flea uses in 1 locality and the number of different host species that can serve as the flea's principal host (i.e. the one supporting the most fleas in a region) among all regions. Also, we observed a strong positive relationship between the taxonomic distinctness of the host species used in 1 locality and that of all known principal hosts among all localities. These relationships held after correcting for potentially confounding phylogenetic influences. We discuss the implications of scale‐independent host specificity and its association with geographical range size and species‐specific patterns of host use.     

Putative speciation events in Lamellodiscus (Monogenea: Diplectanidae) assessed by a morphometric approach

In the present study, we used morphometry as a proxy to study the microevolution of generalist Lamellodiscus (Monogenea, Diplectanidae) species, comprising gill parasites of sparid fish. We investigated 147 individuals, belonging to nine described species, regrouped in four morphotypes. Morphometric measurements were taken on sclerotized parts of the attachment organ. The formation of groups on the basis of the global morphometry within a host species, or between several host species, was assessed using both exploratory analyses (principal component analysis and clustering analysis) and statistical tests. We showed that: (1) for three out of four morphotypes, the global morphometry was significantly different according to host species used, and (2) the coexistence of two populations of Lamellodiscus elegans on Diplodus sargus could reflect an ongoing intra‐host speciation event. We suggest that generalist Lamellodiscus are undergoing specialization on their different hosts, which may lead to speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 559–569.     

我国内陆水体单殖吸虫的宿主特异性分析

报道我国内陆水体单殖吸虫的宿主特异性的研究。研究表明单殖吸虫有很强的宿主特异性,但不同种类的特异的有很大的判别。从目前已有的记录来看,６０％以上的单殖吸虫中只有１种宿主,约７５％的单殖吸虫的宿主仅为１属,超过９７％的单殖吸虫的宿主在１科之内。没有１种单殖吸虫可生于超过３个料的宿主中,但大钩指环虫可在２３属３３种宿主中寄生。在科和发放持异性水平,以锚首虫科和指环虫科单殖吸虫的特异性较强,三代虫科次之     

Are all species of Pseudorhabdosynochus strictly host specific? — A molecular study

Species of the diplectanid monogenean genus Pseudorhabdosynochus are strictly host-specific (specialist), with the exception of P. cyanopodus, which was reported in New Caledonia, South Pacific, from two host species, Epinephelus cyanopodus and E. chlorostigma. We sequenced the COI gene of both host fish species and of their monogeneans. Morphological identification and pairwise distances showed that the two fish species were distinct (difference 6.1-6.6%), but that their monogeneans were not (difference 0-1.5%). A morphological study of sclerotised parts showed that specimens of P. cyanopodus are similar in both fish. Most species of groupers and their associated Pseudorhabdosynochus species are from warm surface waters, but the two groupers E. cyanopodus and E. chlorostigma are usually caught in deep-sea on the outer slope of the coral reef. This suggests that acquisition of a less strict host specificity is an adaptation of P. cyanopodus to deep-sea hosts.     

Generalists versus specialists in fluctuating environments: a bet-hedging perspective

Bet-hedging evolves in fluctuating environments because long-term genotype success is determined by geometric (rather than arithmetic) mean fitness across generations. Diversifying bet-hedging produces different specialist offspring, whereas conservative bet-hedging produces similar generalist offspring. However, many fields, such as behavioral ecology and thermal physiology, typically consider specialist versus generalist strategies only in terms of maximizing arithmetic mean fitness benefits to individuals. Here we model how environmental variability affects optimal amounts of phenotypic variation within and among individuals to maximise genotype fitness, and we disentangle the effects of individual-level optimization and genotype-level bet-hedging by comparing long-term arithmetic versus geometric mean fitness. For traits with additive fitness effects within lifetimes (e.g. foraging-related traits), genotypes of similar generalists or diversified specialists perform equally well. However, if fitness effects are multiplicative within lifetimes (e.g. sequential survival probabilities), generalist individuals are always favored. In this case, geometric mean fitness optimization requires even more within-individual phenotypic variation than does arithmetic mean fitness, causing individuals to be more generalist than required to simply maximize their own expected fitness. In contrast to previous results in the bet-hedging literature, this generalist conservative bet-hedging effect is always favored over diversifying bet-hedging. These results link the evolution of behavioral and ecological specialization with earlier models of bet-hedging, and we apply our framework to a range of natural phenomena from habitat choice to host specificity in parasites.     

Genetic differentiation across North America in the generalist moth Heliothis virescens and the specialist H. subflexa

The two moth species Heliothis virescens (Hv) and H. subflexa (Hs) are closely related, but have vastly different feeding habits. Hv is a generalist and an important pest in many crops in the USA, while Hs is a specialist feeding only on plants in the genus Physalis. In this study, we conducted a comparative population genetic analysis to assess whether and how generalist and specialist life styles are reflected in differences in population structures. In Hv 98% of the total variation occurred within populations. The overall differentiation (F(ST) ) between regions was 0.006 and even lower between years (0.0039) and hosts (0.0028). Analyses of population structure suggest that all individuals form one genetically homogeneous population, except for at most 12 individuals (6%) that diverged from this cluster. Population homogeneity likely results from the high mobility of Hv and its generalist feeding behaviour. Hs exhibited substantially more population structure. Even though 96% of the total variation was attributable to within-population variability, F(ST) -values between Hs populations were 10 times higher than between Hv populations. Hs populations showed significant isolation by distance. Analyses of Hs population structure suggest at least two subpopulations and thus some degree of metapopulation structure. We speculate that the patchy distribution of Physalis- the exclusive food source of Hs - contributes to differences in population structure between these closely related species. The finding that the specialist shows more population differentiation than the generalist corroborates the notion that host specialization is not an evolutionary dead end but a dynamic trait.     

Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea)

The evolution and determinants of host specificity in Lamellodiscus species (Monogenea, Diplectanidae) were investigated. The 20 known Mediterranean species were studied, all parasites of fishes from the family Sparidae (Teleostei). An index of specificity, which takes into account the phylogenetic relationships of their fish host species, was defined. The link between specificity and its potential determinants was investigated in a phylogenetic context using the method of independent contrasts. Host specificity in Lamellodiscus species appeared to be highly constrained by phylogeny, but also linked to host size. Mapping specificity onto the parasite phylogenetic tree suggests that specialist species do not represent an evolutionary dead end, and that specialization is not a derived condition. It is hypothesized that the ability to be generalist or specialist in Lamellodiscus is controlled by intrinsic, phylogenetically-related characteristics, and that specialist species tend to use large hosts, which may be more predictable.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 431−443.     

Resource tracking in North American Telorchis spp. (Digenea: Plagiorchiformes: Telorchidae)

We examine the evolution of host specificity for species of Telorchis, using the methods developed by researchers studying phytophagous insect-plant systems. Optimization of "generalist" compared with "specialist" onto the phylogeny for Telorchis revealed ambiguous patterns, depending on how the 2 terms were defined. Regardless of that definition, most of the evolutionary diversification of this group has been carried out within eucryptodiran turtles, the ancestral host group. From that plesiomorphic background, there appears to have been 2 episodes of specialization by way of a host switch into caudates (ancestor of T. stunkardi + T. sirenis) and snakes (T. auridistomi), and 1 episode of exuberant expansion producing a true generalist (T. corti). These results, which indicate that most species of Telorchis are tracking widespread plesiomorphic resources, mirror those reported for phytophagous insects and their plants. We believe that establishing a dialogue between the two research groups will be mutually beneficial to both and will strengthen our understanding of the complex factors underlying the evolution of coevolutionary associations.     

Host specialization is ancestral in Torymus (Hymenoptera,Chalcidoidea) cynipid gall parasitoids

The host range of parasitoids varies greatly among species: Some only parasitize one to a few hosts (specialists), while others parasitize multiple species or a variety of host types (generalists). The direction of most host range shifts in parasitoid groups, that is from generalist to specialist or, alternatively, from specialist to generalist, is unknown. To explore the origin of host range shifts, we studied a clade within the genus Torymus (Hymenoptera, Chalcidoidea) that includes both generalist and specialist parasitoids of Cynipidae (Hymenoptera). We analysed the phylogenetic relationships of the species of Torymus on the basis of two gene fragments (cox1 and ITS2) of 246 specimens and performed an ancestral state reconstruction of the specialist/generalist trait. Our results revealed the following: (a) The ancestral state of this group of Torymus is specialist, with the generalist state evolving through a loss of specialization. (b) The species Torymus cyaneus and Torymus flavipes both have a strong genetic structure, suggesting the existence of different biological identities. (c) There has been a host plant shift in the lineage(s) leading to Torymus rubi and Torymus bedeguaris from galls on Quercus to those on Rosaceae. (d) The alien species Torymus sinensis and the native European species Torymus notatus are phylogenetically closely related. (e) Speciation within Torymus was likely associated with the diversification of their cynipid hosts, which itself was driven by the dramatic changes in climate and vegetation that occurred during the Miocene.     

Electroantennogram (EAG) responses of Microplitis croceipes and Cotesia marginiventris and their lepidopteran hosts to a wide array of odor stimuli: Correlation between EAG response and degree of host specificity?

In order to test whether the electroantennogram (EAG) response spectrum of an insect correlates to its degree of host specificity, we recorded EAG responses of two parasitoid species with different degrees of host specificity, Microplitis croceipes (specialist) and Cotesia marginiventris (generalist), to a wide array of odor stimuli including compounds representing green leaf volatiles (GLVs), herbivore-induced plant volatiles (HIPV), ecologically irrelevant (not used by the parasitoid species and their hosts for host location) plant volatiles, and host-specific odor stimuli (host sex pheromones, and extracts of host caterpillar body and frass). We also tested the EAG responses of female moths of the caterpillar hosts of the parasitoids, Heliothis virescens and Spodoptera exigua, to some of the odor stimuli. We hypothesized that the specialist parasitoid will have a narrower EAG response spectrum than the generalist, and that the two lepidopteran species, which are similar in their host plant use, will show similar EAG response spectra to plant volatiles. As predicted, the specialist parasitoid showed greater EAG responses than the generalist to host-specific odor and one HIPV (cis-3-hexenyl butyrate), whereas the generalist showed relatively greater EAG responses to the GLVs and unrelated plant volatiles. We detected no differences in the EAG responses of H. virescens and S. exigua to any of the tested odor.     

Host-parasitoid association and diffuse coevolution: when to be a generalist?

In host-parasitoid communities, hosts are subjected to selective pressures from numerous parasitoid species, and parasitoids may attack several host species. The specificity of host resistance and parasitoid virulence is thus a key factor in host-parasitoid coevolution. A continuum of strategies exists, from strict specificity to a generalist strategy. The optimal level of specificity may differ in host and parasitoid. I investigated the optimal level of resistance specificity using a model in which the host could be attacked by two parasitoid species, with variable levels of defense specificity. The fitness of a parasitoid attacking two host species with different levels of virulence specificity was also modeled. Finally, a fluctuating environment was simulated by introducing variable probabilities of encounters between antagonistic species over several generations. If the frequency of encounters with the antagonistic species is fixed, then both host and parasitoid gain from a strategy of exclusive specialization toward the most frequent antagonist. If the frequency of encounters fluctuates between generations, generalist host resistance and partially specialist parasitoid virulence are favored. Generalist host resistance may be considered to be a bet-hedging response to an unpredictable environment. This asymmetry in host-parasitoid coevolution may account for some of the genetic structures observed in the field for host-parasitoid associations.     

How many species of host-specific insects feed on a species of tropical tree?

The assumptions on the host specificity of beetles that led Terry Erwin to suggest that there may be over 30 million arthropod species were tested for 10 species of trees and their insect associates at a rainforest site in Papua New Guinea. The data included 391 species and 4696 individuals of herbivorous beetles collected during a one year period using hand collecting, beating, branch clipping, intercept flight traps and pyrethrum knockdown. Insect host specificity was assessed by feeding trials in captivity. The data suggest that between 23 and 37 monophagous leaf-feeding species are most likely to be present in this system, whereas Erwin's method yields an estimate of 138 monophagous species. The major factors responsible for the discrepancy between our observations and Erwin's assumptions appears to be (a) the importance of transient species; (b) the insect fauna that is shared among tree species; (c) some generalist wood-eating species may inflate the apparent species richness of leaf-feeding beetles; and (d) the proportion of specialist species varies significantly among tree species. We conclude that studies reporting the proportion of specialist insect herbivores associated with particular tropical tree species will yield only a portion of the information needed to estimate global arthropod species richness, but may be useful for elucidating certain aspects of food-web ecology in tropical rain forests.     

Niche width impacts vertebrate diversification

Aim The size of the climatic niche of a species is a major factor determining its distribution and evolution. In particular, it has been proposed that niche width should be associated with the rate of species diversification. Here, we test whether species niche width affects the speciation and extinction rates of three main clades of vertebrates: amphibians, mammals and birds. Location Global. Methods We obtained the time‐calibrated phylogenies, IUCN conservation status, species distribution maps and climatic data for 2340 species of amphibians, 4563 species of mammals and 9823 species of birds. We computed the niche width for each species as the mean annual temperature across the species range. We estimated speciation, extinction and transition rates associated with lineages with either narrow (specialist) or wide (generalist) niches using phylogeny‐based birth–death models. We also tested if current conservation status was correlated with the niche width of species. Results We found higher net diversification rates in specialist species than in generalist species. This result was explained by both higher speciation rates (for the three taxonomic groups) and lower extinction rates (for mammals and birds only) in specialist than in generalist species. In contrast, current specialist species tended to be more threatened than generalist species. Main conclusions Our diversification analysis shows that the width of the climatic niche is strongly associated with diversification rates and may thus be a crucial factor for understanding the emergence of diversity patterns in vertebrates. The striking difference between our diversification results and current conservation status suggests that the current extinction process may be different from extinction rates estimated from the whole history of the group.     

Host specificity of monogenean ectoparasites on fish skin and gills assessed by a metabarcoding approach

Monogeneans are highly diverse fish ectoparasites with a direct life cycle, widely distributed, and are known to generally display strict host specificity. Factors related to the hosts and the parasite have been suggested to explain this high specificity. Monogeneans have also been observed to colonise fish species not in their natural host range under experimental conditions. We developed a specific metabarcoding protocol and applied it on the Sparidae-Lamellodiscus host-parasite system, to assess parasite diversity on skin and gills of several sparid host species. We first demonstrated that the use of a metabarcoding approach provided a better understanding of the diversity of monogeneans associated with teleost skin and gills than traditional approaches based on morphological identification. We identified a high diversity of both expected and unexpected (never observed on this host species) Lamellodiscus spp. on each host species and on skin and gills. No significant difference in parasite diversity was found between skin and gills. These results suggest that the establishment of the observed host specificity in monogeneans relies on multiple levels of regulation, involving the survival capacity of the larvae and host recognition mechanisms.     

Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

Host-parasite associations and host-specificity in haemoparasites of reed bed passerines

The host specificity and host sharing of avian haemoparasites (genera Haemoproteus and Plasmodium) is still poorly known, although they infect a large proportion of several studied bird populations. This study used molecular techniques to detect haemoparasites in marsh warblers and in other passerines that feed in reed beds, at 4 sites in Portugal. The host-specificity of the parasite lineages was analysed and compared with other cases described in the literature to assess whether apparent host specificity changes according to the studied system. Nine lineages of Haemoproteus and 15 of Plasmodium were found, of which only 10 Plasmodium were proven to have local transmission. Each lineage was confined to a distinct set of host species. The distribution of parasites in the host species was non-nested, meaning that specialist lineages did not always share hosts with generalists. The most prevalent lineages were those with a wider host range, indicating that the ability to infect more hosts will enhance a parasite's prevalence in its entire host range. We also found that in our areas, a specialist parasite (H. MW1) appears to have a more generalist character than described in the literature, suggesting that a parasite's apparent specialization can depend on the type of host species sampled.