4.3 The mechanism of parasitic intersexuality
4.3.2 Interference in insect sexual differentiation or juvenilization
Mechanism of how a parasite manipulates the host phenotype is critical to further understand its adaptation (Poulin, 1995). It has long been known that horsehair worms and their ecological closed mermithids frequently cause the intersexuality in their hosts (Metrioptera brachyptera, Pholidoptera sp., Pterostichus niger, Blaps
mucronata, Vespa germanica (Wülker, 1964), midges (Chironomidae) (Rempel, 1940;
Wülker, 1985), biting midges (Ceratopogonidae) (McKeever et al., 1997),
grasshoppers (Acrididae) (Rowell, 2000), mayflies (Baetidae) (Vance, 1996), and mantids(Roy, 2003)), but it has almost never been mentioned how these parasites
interfere in the insect sexual differentiation.The common coexistence of the gonad destruction (castration) and the intersexuality (Baudoin, 1975) makes the sexually dimorphic characteristics in the infected host are believed to be altered due to the loss of stimulus produced by sex glands
(e.g. Rempel, 1940). Such hypothesis is known as juvenilization, which
keeping host characters in the early step of ontogeny (Baudoin, 1975; Hurd, 2009) and well explains the parasitic cases of the infected mammals (Vainio et al., 1999) and infected crustaceans (Rodgers-Gray et al., 2004). However, despite the "androgenic gland" has found in some arthropods (crustaceans)(Rodgers-Gray et al., 2004), it is
still under debate that if the insect sexual differentiation is the "cell-autonomous process"(Negri and Pellecchia, 2012). It is traditionally believed that every cell
decides for itself what its sexual phenotype should be (DeFalco et al., 2008). One of the evidence is the gynandromorph due to the incomplete cell division and consequently causes an insect individual mosaically contains both male and female characteristics (Negri and Pellecchia, 2012). The gynandromorph in a certain extent rejects the existence of sex hormone which has not detected in any insect species (deLoof and Huybrechts, 1998; Negri and Pellecchia, 2012). It is recently challenged by
the finding of the avian gynandromorph (Bear and Monteiro, 2013) and the inter-cell regulating factor in the embryogenesis of Drosophila(DeFalco et al., 2008).
Nevertheless, it is still less evident of the factor regulating the insect sexual differentiation especially in the post embryonic development.
The lack of factors regulating insect sexual differentiation leads the "parasitic juvenilization" limited to its literal meaning. The juvenilization is still noted in the parasite-infected insect hosts by means of increasing the juvenile hormone titer and makes the juvenilized characteristics on the host (Fisher and Sanborn, 1962; Down et
al., 2008; Hurd, 2009). In some cases, the juvenilized characteristics cause the same
phenomenon of the intersexuality since the sexual dimorphism in insects is sometimes resulted from development of the structures in one of the sex and maintenance of the juvenile form in alternative sex
(de Loof and Huybrechts, 1998). The "general
juvenilization" might be supported by the non-change in the female antenna of H.formosana since it maintain the same characteristic with the last instar nymph (Fig.
15A; Chiu et al., 2015). However, this phenomenon does not exclude the possibility
that the horsehair worm interferes in insect sexual differentiation to lead the "female developmental process" in the infected male. In addition, the antennal characteristic of the infected male H. formosana is not totally juvenilized which is morphologically different from its last instar nymph but similar to the female (Fig. 15A; Chiu et al.,2015).
These two hypothesis (interference in insect sexual differentiation and general juvenilization) could cause the same phenomenon of intersexuality, but indicate different developmental processes that the horsehair worm might intervene during infection. Under the hypothesis of the general juvenilization, the antennal
characteristic is not changed in the female H. formosana since it maintain the nymphal characteristic. Thus, there is two main points in the hypothesis testing: After the horsehair worm begin to manipulate host development, 1) if the infected females are still not affected (even they do not maintain the nymphal characteristics in the adult of H. patellifera), and 2) if the sensillum distribution of the infected male stop developing in each nymphal instar.
It should be first realized the beginning of the time when the horsehair worm start to manipulate host development after the cyst enters the mantids. The morphology of insect stop changing after the last molting. After this time point (the last molting), the horsehair worm effect on the host development will not be displayed on the host morphology. In other word, if the horsehair worm cyst enter the mantids
"too late", the infected male will show the normal antennal instead of the feminized one. This phenomenon was found on the H. patellifera artificially infected by
Chordodes sp., while the parasitic effect on the host antennae is significantly
correlated with the span of time between the time of host last molting and ingestion of the horsehair worm cyst (Appendix 5). The infected mantids with longer developmental time spans before the last molting tend to have the manipulated antennae (Fig. 25, 26). With the estimation by the logistic regression model, the horsehair worm's effect begins at around 36 (95%CI: 32.24-40.53) days (90% of the host start to change the morphology) after the cysts are ingested (Fig. 26). In addition to the change in the antenna, few infected males (6 individuals) were also found to show the red pigments on abdomens 32 days after being infected (Fig. 21B, C). These results suggest the horsehair worms start to manipulate the host development at around 30 to 36 days, which is around the first one-third of their developmental period (the total developmental days of our artificial infected C. formosanus is 97 ±22 days (54-143 days, n = 18)).
Fig. 25. Sensillum distributions (the antennal segment first bearing the grooved basiconic sensilla) in the adult male mantid, Hierodula patellifera, of the control mantids and that infected by the horsehair worm, Chordodes sp. Y-axis is the first flagellum segment bearing the grooved basiconic sensilla. X-axis is developmental time between the date of infection and the last molting. The box-plots are the values of the control mantids (left, n = 11) and the infected mantids (right, n = 26). The dots are values the infected mantids against the developmental time. The dash lines indicated the first and second standard deviations of the control value, which separates the infected hosts into non-manipulated group (black dots), manipulated group (red dots), and three individuals which are removed from analysis conducted by the logistic regression model (hollow dots).
Fig. 26. The begin time when the horsehair worm, Chordodes sp., start to manipulate the development of the mantid, Hierodula patellifera. Y-axis is the appearance of parasitic effect on the host antennae against the time span between the date of infection and the last molting (X-axis). The black line is the regression line estimated by logistic regression model. Red dot and black dot are 50% and 90% individuals been manipulated, respectively, estimated by the logistic regression model with one standard deviation.
The estimation of logistic regression model suggests more than 90% of the infected host will show the manipulated morphology 36 days after being infected. In the artificial infection of H. patellifera and Chordodes sp., 12 of 14 infected male developed for more than 30 days and all the seven infected male developed for more than 36 days after being infected displayed the manipulated antennae. Under the hypothesis of general juvenilization, the male nymph and the female adult are expected to also show the juvenilized antennae 36 days after being infected.
Unfortunately, in this dissertation we not yet have a very clear conclusion supported by enough samples, but the few samples make me to believe the horsehair worms interfere in the host sexual differentiation instead of the juvenilization. In the same
(three of them are more than 36 days) after the infection but all showed the normal antennae (Fig. 27). The similar situation is also happened in the infected female adult.
In the samples we have in these few years, five infected females also showed the normal antennae which are not juvenilized by the infection since their significantly different sensillum distribution from that of the last instar nymph (Fig. 28).
Now the samples is still not enough to support a very clear conclusion.
Nevertheless, these few samples makes it is worth to keep testing if the horsehair worms interfere in the host sexual differentiation. In addition, these samples also suggest the much more complex parasitic effect than our previous thinking. In the artificial infection, the "manipulated host" shows the significantly increased level of the parasitic effect which makes the distribution of the sensilla shifts toward the posterior of antennae with the increasing developmental time (Linear regression model:
β = 0.37, t = 2.63, P = 0.02) (Fig. 25, red points). This increasing parasitic
effect implies the gradually diverged process in the host sexual differentiation.However, the differentiation of the sensilla distribution of H. patellifera is only happened during the last molting instead of gradually diverge in each nymphal instars.
The gradual antennal change might be caused by the accumulation of parasitic effect on the time point of the host sexual differentiation, but this explanation still needs more evidence to be confirmed.
Fig. 27. Sensillum distributions (the antennal segment first bearing the grooved basiconic sensilla) in the last instar male mantid, Hierodula patellifera, of the control mantids and that infected by the horsehair worm, Chordodes sp. Y-axis is the first flagellum segment bearing the grooved basiconic sensilla. X-axis is developmental time between the date of infection and the penultimate molting.
The box-plots are the values of the control mantids (left, n = 13) and the infected mantids (right, n = 23). The dots are values the infected mantids against the developmental time. The dash lines indicated the first and second standard deviations of the control value, while all the infected values fall inside the range of two standard deviations of the control mantids.
Fig. 28. Developmental trajectories of the sensillum distribution (the antennal segment first bearing the grooved basiconic sensilla) on mantid antennae,
Hierodula petallifera and the female individuals (red dots, n = 5) infected by
the horsehair worm, Chordodes sp. or C. formosanus. The 10th instar is the adult stage.5 Conclusion
The ten-year study in this dissertation is the first systematic investigation of the horsehair worm in Taiwan. Here we preliminarily reveal the five Taiwanese horsehair worm species. The two most common species Chordodes formosanus and
Acutogordius formosanus n. sp., which are relatively easy to be collected and cultured,
might be the model species in the advanced studies. The Gordius sp., despite its narrow distribution in mid-altitude mountains and unknown definitive host, might adopt the special adaptation which has never been revealed among the horsehair worm. Besides, several species are still not described in Taiwan.The developmental manipulation in the mantid host infected by C. formosanus open the newly known host-parasite interaction in the horsehair worm's parasitism.
Our current evidences suggest the Chordodes horsehair worms is likely to interfere in the sexual differentiation of its mantid host. This hypothesis provides a new evidence to challenge the traditional belief of the cell-autonomous process. In addition to collect more infected samples to test the hypothesis of the interference in insect sexual differentiation and general juvenilization, the regulating factor in the insect sexual differentiation and parasitic effect is the most attractive issue in the horsehair worm-mantid system. One possible factor is the mimetic Wnt proteins produced by the horsehair worm. From early 20th century, comparison of protein expression has been applied to reveal the possible mechanism in horsehair worm's manipulation.
Biron et al. (2005b, 2006) found two Wnt proteins inside the horsehair worms were
sequencely similar to the insects rather than their phylogenetic-related nematode,Caenorhabditis elegans. These similarity made them believed to be functional in
physiological regulation of their host as that explaining in the concept of molecularevolutionary advantage of molecular mimicry can be easily understood, parasitoproteomics tells us only the difference of protein expression, whereas the consequences of mimicry on pathogenesis are still unclear (Salzet et al., 2000). The mimetic Wnt proteins found inside the horsehair worms are originally strongly believed to be the factor manipulating the host behavior, but their function has not been confirmed to date
(Biron and Loxdale, 2013). Wnt gene is the conserved genes
appearing in metazoan animals and named after the Drosophila segment polarity gene,wingless, and the vertebrate homolog, integrated. Its expressed protein acts as
extra-cellular signal stimulating internal-cellular signal transduction cascades and consequently regulates several aspects of developments including the cell fate determination(Komiya and Habas, 2008). In the recent study of embryogenesis in
Drosophila gonad, the Wnt2 gene was found to be the key factor in regulating the
sexual differentiation of Drosophila gonads (DeFalco et al., 2008). It is likely that the mimetic Wnt proteins produced by the horsehair worms cause the intersexuality in the infected host. It is worth to keep promoting the understanding in the mechanism of the horsehair worm-induced intersexuality before the technique is advanced enough to conduct the biochemical experiments.6 References
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