Xenopsylla ramesis

There is no parasite that is universally infective, even generalist parasites that can infect many different host species are usually limited to a particular taxonomic group - such as fish, insects, or mammals. Some parasites may infect a broad spectrum of hosts during one stage of their life-cycle, but are very specific in another. For parasites that are host specialists, this can be taken to an extreme level where they are found exclusively on just one particular host species. Just how parasites evolve from generalist to become so specialised is one of the enduring questions in studies of the evolutionary ecology of parasites.

Image from of the related and more well-known
Xenopsylla cheopis (also known as the plague flea)
from the NHM

To investigate this question, a group of scientists from Israel carried out an experiment on Xenopsylla ramesis - a species of flea that infects a number of different desert rodents. For their experiment, the scientists raised separate populations of fleas on two species of desert rodents - Wagner's Gerbil and Sundeval's Jird - both of which are commonly infested with X. ramesis in the wild. Each of the experimental flea populations were assigned to either gerbils or jirds, and raised for nine consecutive generations on their specifically assigned rodent species. Out of every generation, the scientists also took a subset of 30-50 fleas from each of the experimental populations, and transferred them onto the other host species to see how those fleas performed compared with their counterparts that got to stay with the specific rodent host that they have been assigned with.

For the first three generations, there were no noticeable differences when the fleas were switched from either gerbils or jirds onto the alternative host. But by the sixth generation, the fleas have become so attenuated to the specifically assigned rodent species that when they were transferred to a host that was different to the one that their parents were raised on, they suffered drastically. Female fleas which had been transferred to the alternative host produced far fewer eggs (only about a quarter of the number produced by fleas that got to stay with their assigned host), and out of those eggs which were laid, fewer of them actually hatched, and out of the larvae that hatched, very only one-quarter to one-fifth reached full maturity.

The scientists who conducted this study suggested that this came about through what is known as "relaxed selection". When the fleas had been infecting multiple host species, there was selection pressure on them to maintain whatever full suite of adaptations that had allowed them to feed off a broader spectrum of hosts. But when the population is restricted to a single host species, there is no longer any selective advantage in maintaining the full suite of traits. Thus the adaptation(s) associated with infecting those other hosts (which they are no longer exposed to) were discarded, leaving only the specific adaptation(s) that are relevant to exploiting the available host species.

Another thing to note is that the natural ability of X. ramesis to live off multiple rodent hosts deteriorated very rapidly - within just a few generations - and the effects were drastic. The authors suggested it might have occurred through epigenetic modifications - inheritable changes in gene expressions which do not involve any changes in organism's DNA sequences (instead of mutations, which alter the underlying structure of the DNA). Another possibility, which the scientists who conducted this study did not raise, is whether the gut microbes of the fleas played a role in their ability to exploit different host, as it has been shown to be the case for some plant pests. However, little is known about the microbes that inhabit flea guts, apart from pathogens that are known to be vectored by fleas such as the bacteria that causes the plague.

Reference:
Arbiv, A., Khokhlova, I.S., Ovadia, O., Novoplansky, A. and Krasnov, B.R. (2012) Use it or lose it: reproductive implications of ecological specialization in a haematophagous ectoparasite. Journal of Evolutionary Biology 25: 1140-1148.

P.S. Don't forget, both Susan and I will be attending parasitology conferences happening on our respective continents in July and we will be tweeting about them - you can find me on Twitter @The_Episiarch and Susan @NYCuratrix. I will be tweeting the Australian Society for Parasitology conference 2-5 July, while Susan will be tweeting the American Society of Parasitologists conference 13-16 July. Follow the hashtag #ASP2012 for relevant tweets. On the 2 July, there will also be a livestream public talk call "Parasite Encounters in the Wild" - Twitter participation is encouraged so feel free to tweet your question with the hashtag #ParasWild during the talk.

Corynosoma cetaceum

image from here

In the last post we met Acanthocephalus rhinensis - an acanthocephalan which lives a pretty normal life (for a thorny-headed worm) - it spends its adult life anchored to the intestinal wall of its eel host, absorbing the nutrient-rich slurry of the intestinal content through its body surface. Today, meet Corynosoma cetaceum - it is yet another acanthocephalan, but that's about where its similarity with A. rhinesis ends. Corynosoma cetaceum lives inside the stomach of dolphins, and it is one prickly customer. As well as having the signature thorny proboscis (see the lower right picture), its entire body is covered with a spiky coat of wickedly-sharp spines (see picture on the upper left showing spines extending well pass the proboscis) which would put a hedgehog to shame.

Whereas in other acanthocephalans the proboscis plays the main attachment role, in C. cetaceum uses its entire body to cling on. The study which forms the basis of today's post looked at differences in the spines of male and female C. cetaceum, and found a high degree of divergence between the sexes. While female worms are smaller, overall they have much longer spines than males. In fact only in females do the spines grow significantly during maturation from larva (known as a cystacanth) to adult. In contrast, the body spines of adult male C. cetaceum remains more or less the same length as they were as cystacanths.

image composed from here and here

This seems odd, because being smaller, the females are actually at less risk of being dislodged (less surface area exposed to the dragging flow of the stomach content) - so why the longer spines? One possibility raised by the researchers is that perhaps the males simply depend upon attachment mechanisms other than body spines - but compared with females, the male worms have smaller proboscis and hooks too. Alternatively (and more likely), perhaps female worms need to stay in the host for longer than the males in order to produce and release eggs. There are indirect data which indicates female C. cetaceum live longer than their male counterpart - this is inferred from what is known for other acanthocephalans, and the sex ratio of C. cetaceum populations found in the stomach of dolphins which is skewed towards having more females.

There are further, as yet unsolved mysteries relating to C. cetaceum. As mentioned at the start of this post, the stomach is a very different habitat to the intestine. The life of parasites living in the intestine is fairly leisurely, being bathed a steady flow of nutrient-rich slush composed of finely-digested food infused with a cocktail of the host's bodily secretions. In stark contrast, the stomach is an extremely harsh environment. It is where early stages of digestion takes place - where chunks of food are mashed up and soaked in harsh digestive juices. The content of the stomach is composed largely of chyme - an acidic mixture of partially digested food and acid which is not all that nutritious for parasites like acanthocephalans which absorb nutrients through their body surface. In addition, carnivorous marine mammals consume huge quantity of food whenever the opportunity arises; this results in unpredictable and heavy flows of food through the stomach which makes for an extremely turbulent environment that can easily dislodge any parasitic worms (see this paper).

Of all the places in the digestive tract that C. cetaceum can occupy, why has this species evolved to live in such an inhospital environment?

Reference:
Hernández-Orts, J.S., Timi, J.T., Raga, J.A., García-Varela, M., Crespo, E.A. and Aznar, F.J. (2012) Patterns of trunk spine growth in two congeneric species of acanthocephalan: investment in attachment may differ between sexes and species. Parasitology 139:945-955.

P.S. Attention parasite appreciators! Both Susan and I will be attending parasitology conferences happening on our respective continents in July and we will be tweeting about them. So as if this blog isn't already enough, you can your 140 characters or less fix of parasitology goodness on Twitter - you can find me on Twitter @The_Episiarch and Susan @NYCuratrix. I will be tweeting the Australian Society for Parasitology conference 2-5 July, while Susan will be tweeting the American Society of Parasitologists conference 13-16 July. 

Acanthocephalus rhinensis

image from figure 1 of the paper

The study which forms the basis of today's post features an acanthocephalan - also known as a thorny-headed worm - which lives in the intestine of European eels in Lake Piediluco in central Italy. Acanthocephalans spend their adult lives like tapeworms, clinging to the wall of their host's intestine, and absorbing nutrients from the pre-digested gut content. But unlike tapeworms, which mostly use suckers and small hooks to cling to the intestinal wall, an acanthocephalan has a formidable bit of armament which puts the tapeworms to shame. As its name indicates, at the front of the acanthocephalan is a hook-laden proboscis (see the picture on the right) to stab into the intestinal wall and firmly anchor themselves in place.

In Lake Piediluco, some eels were found to be infected with up to 350 Acanthocephalus rhinensis, though most eels had fewer than 50 worms. The eels become infected through eating little shrimp-like crustaceans called amphipods. The amphipods live mostly amongst the aquatic vegetation at the edge of the lake, and they are parasitised by the larval stage of A. rhinensis. If you thought the idea of having dozens of prickly-headed worms clinging to your intestinal wall with their nightmarish probosces is bad, A. rhinensis is downright brutal to the amphipod host.

image from figure 3 of the paper

The larval worm (called a cystacanth) occupies a large part of the little crustacean's body (see picture on the left), displacing many of its internal organs. About one in ten amphipods at Lake Piediluco are infected with A. rhinensis, and each amphipod had one or two worms inside them (probably because there wouldn't be much room for more). Acanthocephalus rhinensis imposes a massive burden on the little crustaceans - infected females can only successfully produce half as many eggs as uninfected females.

Armed with that formidable anchor, you would think that A. rhinensis would be able to establish itself in the gut of just about any fish it finds itself in. But it appears to be remarkably faithful to eels, which are the only fish found to have A. rhinensis in their intestines. Perhaps there are other immunological or ecological reasons that prevent this species from successfully infecting other fish.

In addition to establishing the life-cycle of A. rhinesis, another discovery made by the researchers actually served to amend an existing error in the scientific literature. In the original description of A. rhinensis, which was made based on nine specimens, this species is supposed to have a distinctive band of orange-brown (think spray-on tan) pigment just behind their proboscis, a feature that apparently distinguishes it from all the other Acanthocephalus species. However, the researchers who wrote this paper examined a total of over a thousand worms and not a single one had the supposed distinguishing band. But what gave those worms that orange-brown collar? The researchers suggested that this was caused by discolouration from being jammed so deeply into the intestinal wall that the worms inadvertently absorbed pigment from host's intestinal vessel which gave them a distinctive tinge just behind their proboscis.

So in addition to working out the life-cycle of A. rhinensis, this study also served to clarify old mistakes, which will help out any future researchers who work on this species.

Reference:
Dezfuli, B.S., Lui, A., Squerzanti, S., Lorenzoni, M. and Shinn, A.P. (2012) Confirmation of the hosts involved in the life cycle of an acanthocephalan parasite of Anguilla anguilla (L.) from Lake Piediluco and its effect on the reproductive potential of its amphipod intermediate host. Parasitology Research 11: 2137-2143.