Cryptic diversity and patterns of host specificity in trematode flatworms

Authors


  • PERSPECTIVE

Alexander Hayward, Fax: 44 1865 310447; E-mail: alexander.hayward@zoo.ox.ac.uk

Abstract

The widespread utilization of molecular markers has revealed that a broad spectrum of taxa contain sets of morphologically cryptic, but genetically distinct lineages (Bickford et al. 2007). The identification of cryptic taxa is important as an accurate appreciation of diversity is crucial for a proper understanding of evolutionary and ecological processes. An example is the study of host specificity in parasitic taxa, where an apparent generalist may be found to contain a complex of several more specific species (Smith et al. 2006). Host specificity is a key life history trait that varies greatly among parasites (Poulin & Keeney 2007). While some can exploit a wide range of hosts, others are confined to just a single species. Access to additional hosts increases the resources available to a parasite. However, physiological or ecological constraints can restrict the extension of host range. Furthermore, there may be a trade-off between relaxed specificity and performance: generalism can decrease a parasites ability to adapt to each individual host species, and increase exposure to competition from other parasites (Poulin 1998). Despite the central role that host specificity plays in parasite life history, relatively little is known about how host range is determined in natural systems, and data from field studies are required to evaluate among competing ideas. In this issue, an exciting paper by Locke et al. (2010) makes a valuable contribution toward the understanding of host specificity in an important group of trematode flatworms. Using molecular methods, Locke et al. reveal an almost four-fold increase in the appreciated diversity of their focal group. In combination with a large and elegant sampling design this allows them to accurately assess host specificity for each taxon, and thus draw key insights into the factors that control host range in a dominant parasite group.

The Digenea (Platyhelminthes: Trematoda) are remarkable organisms. Perhaps their most striking feature is the complex life cycles that characterize the group. For example, some have as many as four hosts, such as the European species Halipegus ovocaudatus (Vulpian 1858), which includes a freshwater snail, a copepod, a dragonfly, and a frog host in its lifecycle (Kechemir 1978). Digeneans are also known for the ability to manipulate their hosts, as demonstrated by the common textbook example of parasitic manipulation, the lancet liver fluke, which induces its intermediate ant host to clamp its jaws onto the tip of a blade of grass to facilitate ingestion by the definitive ungulate host. In addition, digeneans are important agents of disease, with millions of people worldwide infected by blood flukes (schistosomes), and many species responsible for serious pathology in a wide range of domesticated and wild animals.

Despite being of considerable interest, many basic questions regarding the evolutionary ecology of the Digenea remain unanswered. This is in no small part due to the challenges involved in studying them. As a result of their endoparasitic lifestyle, gathering specimens requires the collection and dissection of potential hosts, and is difficult and time-consuming (Fig. 1). Furthermore, species identifications, which are usually based on morphology of the adult stage, may be problematic. Digeneans are small, soft bodied, can have a paucity of good taxonomic characters, and may be subject to age or host-induced phenotypic plasticity (Nolan & Cribb 2005). These difficulties are accentuated for the metacercaria, a morphologically reduced larval resting stage that occurs in the second intermediate host, which can be virtually impossible to identify using traditional methods (Fig. 2). Thus, relatively little is known about the true diversity or host specificity of many groups of digeneans, particularly at the level of the metacercaria.

Figure 1.

 Gathering metacercariae requires the collection of potential hosts. Here fish are being sampled using a beach seine at Iles aux Sables, Lake St. Pierre, on the St. Lawrence River, Canada (Photo credit: Sean Locke).

Figure 2.

 Encysted Posthodiplostomum metacercariae present in a squash preparation of the liver of a 1-year-old pumpkinseed (Lepomis gibbosus) (Photo credit: Sean Locke).

Locke et al. tackle the issue of cryptic diversity and host specificity in metacercariae of the Diplostomoidea. In this superfamily, metacercariae parasitize fish, providing a bridge between the molluscan first intermediate host and the definitive host, which is typically a piscivorous bird. Locke et al. uncover substantial cryptic diversity and provide evidence that suggests the majority of species are highly host specific, with the exception being diplostomoids occurring in the lens within the eye of fish hosts. The authors make a convincing argument that a physiological mechanism is responsible for the observed pattern, suggesting that relaxed host specificity in the lens may be attributable to a limited immune response at the site. In doing so, they provide much needed field data, and present an important hypothesis to explain the pattern of host specificity in the Diplostomoidea.

The ability of Locke et al. to draw these insights lies in the careful and precise manner in which they undertook their study. First, they implemented appropriate molecular techniques to overcome the taxonomic difficulties associated with studying digeneans, utilizing both a high-resolution mitochondrial and a nuclear marker. Importantly, in doing so, they did not pool parasite specimens despite the small tissue sizes often encountered. Second, their sampling design was elegantly replicated, and specificity was quantified using a range of statistics accounting for potentially confounding factors. This approach ensured that the relative influences of ecology and phylogeny could be teased apart with high power.

Host specificity is a more complex character to quantify than it can at first appear. Its most basic measure is host range, being simply the number of species from which a given parasite is recorded. However, this interpretation is misleading because it considers all hosts as equal, which is typically an inaccurate assumption. Phylogeny is one important variable by which hosts may differ, as closely related species generally share a greater proportion of life history traits than distantly related species (Harvey & Pagel 1991). Thus, parasites considered to possess low host specificity should be able to exploit hosts from a broad taxonomic range. In order to quantify host specificity more accurately, Locke et al. utilized two indices that take taxonomic diversity into account. This is significant, as despite the importance of phylogenetic relatedness among hosts, few other studies have implemented these indices to date.

Locke et al. balanced the contribution of phylogeny against potential ecological effects on host specificity by selecting a focal host set comprising both closely related but ecologically different, and ecologically similar but more distantly related species. In order to test if ecological conditions at the sampling site exerted an effect on specificity, samples were replicated at six sites that expressed key ecological differences. During analysis, the authors were careful to consider sampling effort, which is an important factor in the accurate interpretation of host specificity (Poulin 1997). Furthermore, a test was also undertaken to examine the influence of parasite phylogeny on the observed pattern of specificity, so that the relationship between infection site in the host and relaxed specificity could be disentangled from relatedness among parasite species.

Finally, the scale of the fieldwork involved in generating the study is impressive and contributed greatly to its potential. In total, over 1000 diplostomoid specimens were sequenced, originating from more than 800 host fish. While a growing number of studies have demonstrated the existence of cryptic species in trematodes, few have carried out the large-scale, well-designed sampling scheme necessary to detect rare species and consider the general patterns accessed here.

Despite the acknowledgement that parasite communities of freshwater fish are well studied in Canada using traditional approaches, Locke et al. uncovered significant cryptic diversity. This finding reinforces the assertion that substantial amounts of parasite diversity may be lost before we are even aware of its existence in the wake of the current threat to global biodiversity (Dunn et al. 2009). In addition, parasites represent a major portion of known global biodiversity and play an important role in a wide variety of ecosystem processes (Windsor 1998; Poulin & Morand 2004). An accurate appreciation of parasite diversity and specificity is crucial for a variety of applications from making evolutionary inferences about host–parasite coevolution to implementing effective biological control. Much remains to be understood regarding the biodiversity of parasites and the pattern and evolution of host specificity. Thorough and carefully constructed studies such as the one presented here by Locke et al. offer the valuable insights necessary for advances to be made.

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