Definitive host phase

The main post-embryonic development of a horsehair worm is launched from the cyst is ingested by the definitive host and finishes when the adult worm leave the host.

During the time, a horsehair worm proceeds metamorphosis from a cyst to become the wormlike juveniles

(Hanelt and Janovy, 2005), rapid increase of the body size (Schmidt-Rhaesa, 2005), and finally become a mature worm (Schmidt-Rhaesa, 2005).

These three stages are respectively associated with three interactions with the host:

determination of the host specificity, parasite's trophic strategy with altering host development, and host behavior manipulation.

The metamorphosis of the cyst is the first step to determine a host to be the definitive host or another paratenic host. Unfortunately, it has never been mentioned about the factors triggering the excysted larvae to proceed metamorphosis. In fact, definitive host data are still lacked in many horsehair worm species since they were frequently described only by the free-living adult collected in the environment (Poinar

and Chandler, 2004) or were artificially infected to the laboratory-reared insects by

field-collected cysts (Bolek et al., 2013a). Unlikely the wide host range in the paratenic host, the definitive hosts of horsehair worms are limited to arthropods mainly including millipedes, orthopterans (crickets, grasshoppers, etc.), beetles, cockroaches, and mantids in freshwater environments (Schmidt-Rhaesa, 2012; Bolek

et al., 2015) and crustaceans in the oceans (McDermott et al., 2010; Schmidt-Rhaesa,

2012). In each species, despite only a few surveys mentioned about the host

specificity (Schmidt-Rhaesa, 2012; Chiu et al., 2011), a horsehair worm seems to only able to develop in one or few species of definitive hosts.

After the metamorphosis to become wormlike juvenile, a horsehair worm go through the rapid growth in host's body cavity. This is the only known trophic stage of a horsehair worm to exploit resource from it host. It is believed that a horsehair worm consumes host non-essential fat and reproductive organs to support its growth

(Lafferty and Kuris, 2012) since these two tissues in the infected hosts are commonly

atrophied (Lafferty and Kuris, 2012; Chiu et al., 2015; but in our observation, the fat

body might be not always reduced in the infected mantids). Nevertheless, there is not

yet an evidence confirmed how a horsehair worm gains nourishment from these tissues. By comparing the morphology of the horsehair worm developing for different time inside the definitive hosts, Schmidt-Rhaesa (2005) suggested the intestine is present and occupies half of the body cavity in the early development of the juvenile.

The intestine maintains its size in the first third of its developmental period and then become smaller (Schmidt-Rhaesa, 2005). In the adult worms, the intestine is almost degenerated

(Schmidt-Rhaesa, 2005). The degeneration of the intestine not only

support the hypothesis that the horsehair worms emerges from the hosts as non-trophic adult (Schmidt-Rhaesa, 2005), but also suggests the juvenile might digest the nutrition through intestine. However,

Schmidt-Rhaesa (2005) in the same report

also suggested the alternative possibility that the horsehair worm directly absorb host nutrition from the "larval cuticle", which covers the juvenile and is much thinner than the fibrous adult cuticle. If the juvenile holding up the resource in the host body flow, the reduction of fat and reproductive organ of host might be not caused by the parasite consumes it but due to the loss of energy or altered development.

No matter how a horsehair worm intake the resource from the host, several reports suggest the infected host suffers the destruction of gonad tissues (Wülker,

1964; Lafferty and Kuris, 2009; Chiu et al., 2015). This effect on the host also makes

the horsehair worm to be categorized as the parasitoids with "prior castration"

(Lafferty and Kuris, 2009). This trophic strategy castrating the host is frequently seen

in the parasitic helminths and insects (Wülker, 1964;

Baudoin, 1975; Hurd, 2001;

Lafferty and Kuris, 2009) whose body size is larger than the usual parasites (Lafferty and Kuris, 2009). It is believed that the rapid growth of these parasites until almost

occupied all the host body cavities is supported by the intensive exploitation of host resource, and thus promotes them consumes the energy invested in host reproductive system to insure their survival, both hosts and parasites (Obrebski, 1975; Lafferty and

Kuris, 2009). The effort to maintain the host survival is the common adaptation of

every parasite, but castrating a semelparous host will deprive it of the heredity contribution to its own population, which is equal to evolutionarily kill it. It is the reason why many of the parasitic castrators finally switch to be a parasitoid and kill the "snatched body". In the parasitism of the horsehair worm, the parasite adopts a unique way to kill and leave the host: forcing the suicide behavior.

Adult horsehair worms reproduce in the water but they are unable to move themselves on the ground. The only way is emerging from the terrestrial host fallen in the water. Parasite-manipulated host behavior is the hot spot of the horsehair worm's

study. It has been noted for more than one century

(Heinze, 1941 reviewed in Schmidt-Rhaesa and Ehrmann, 2001) but has been systematically researched in the

recent 10 years. The "suicide behavior" in the horsehair worm-infected host has been frequently reported as field observation until the first control experiment was conducted by Thomas et al. (2002). It has long been believed that the horsehair worms cause the hosts thirsty and promote them to approach water (Schmidt-Rhaesa

and Ehrmann, 2001), but the behavior of "searching the water" was not supported in

the Y-maze (Thomas et al., 2002).

Thomas et al. (2002)

found both infected and non-infected crickets were randomly choosing one direction of the Y-maze whatever if the arm contained the trough filled with water or not. The similar behavior was also found in the infected crickets which were brought from their forest habitat to the open area near a pool, while only half of individuals moved toward the pool (Thomas et al.,

2002). These two experiments suggested the infected host just moving around instead

of searching and heading the water, but this behavior is still abnormal for a cricket since it always quickly hides itself back to the dark area or forest habitat (Thomas et

al., 2002). This "erratic behavior" is the reason why the infected crickets are always

found in the non-habitat area, like parking area or ground in the house (Thomas et al.,

2002), and further suggested as the first step of the host behavior manipulation caused

by the horsehair worm (Sánchez et al., 2008b). The second step is to make the infected host to "suicide" when it encounters the water. Thomas et al. (2002) in the same Y maze experiment found that all the infected crickets, although they showed no tendency to the direction with water, jumped into the water if they randomly go into the arm with water. Whereas most of the non-infected crickets (11/12) just stopped near the edge of the trough. This phenomenon confirms the "suicide behavior" long spread as a legend. After ten years, Ponton et al. (2011) found the tendency of

approaching reflection of light in the infected crickets, which suggests the "suicide behavior" is likely to be the attraction of light reflected by the water.

The two-step behavior manipulation composed of "erratic behavior", which causes the infected host leaves its habitat, and "suicide behavior", which promotes the host jump into the water, has been generally established. Now scientists are still striving for realizing the physiological mechanism behind these behavior changes.

Several physiological changes have been noted. Thomas et al. (2003) found the infected crickets displayed abnormal concentration of several amino acids and increasing mitosis in mushroom bodies. Biron et al. (2005a) and

Biron et al. (2006)

noted the infected katydids and crickets showed the similar proteomic changes when performing the erratic behavior. These proteins are related to insect's neurogenesis, circadian rhythm and neurotransmitter activities. To date, expression of at least six protein families whose function are related to the physiological processes of insect's central nervous system have been known to change during the behavior manipulation

(Libersat et al., 2009). Two of the proteins belonged to Wnt family is likely to be the

special case of molecular mimicry since the protein sequences in the horsehair worm is similar to that in insects instead of the phylogenetically close nematodes (Biron et

al., 2005a, 2006; Biron and Loxdale, 2013). It is once believed we are nearly to the

answer of the molecular cross-talk between horsehair worms and their hosts, but the linkage of these physiological changes to the host behavior is still unclear (Biron and

Loxdale, 2013). In addition, more parasitic effects induced by the horsehair worms

found in the recent years including the nymphal appearance on the infected female adult crickets (Biron et al., 2005b), morphological allometry and intersexuality in the infected adult mantids (Chiu et al., 2015). The coevolution of the horsehair worms with their definitive hosts has proceeded since early Early Cretaceous

(Poinar and

Buckley, 2006; Bolek et al., 2015) and creates the complex interaction to each other.

Many of the old myths have been understood now, but more will be created with the future studies.

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