rarely seen on the non-infected individuals. These phenotypical changes, which is expressed from parasite genotype but displays on the host (extended phenotype in
Dawkins, 1982), visualizes the adaptation of the parasites by creating the new
function on the manipulated structures or as the symptom showing the host physiological change(Poulin and Thomas, 1999). Both of the functional structures
and the symptom are equally important to understand the living strategy of hosts and parasites. Only under the great interest in the new function created by the parasite's extended phenotype, significance of the symptoms are sometimes overlooked or mislinked to an imaginary functional adaptation (Poulin, 2000).The morphological manipulation have previously been observed in the horsehair worm-infected hosts by the abnormal genitalia in katydids
(Wülker, 1964), the
extreme shorter wing in a male mantid (Roy, 2003), and the nymphal appearance in the adult female crickets (Biron et al., 2005b). In our study, the field-collected mantids, H. formosana, infected by the horsehair worm, C. formosanus, displays the abnormal characteristics including the allometry in the legs and wings, and the intersexuality which found in the infected males (Fig. 12, 13) (Chiu et al., 2015). The allometric morphology comes from the different ratio in the decrease of the walking legs and wings to the pronotum, which create the mantids with short legs and wings, but in the fore-leg (raptorial leg), the parasitic effect is not significant (Fig. 12). Theintersexuality, which is defined as the change of sex characters in which clear signs of the opposite sex can be recognized (Wülker, 1964; Baudoin, 1975), happened on the fore-wing shape and distribution of the antennal sensilla of the infected adult males.
Fig. 12. Sexual dimorphism and parasitic effects of the horsehair worm (Chordodes
formosanus) on the legs and wing lengths of infected mantids (Hierodula
formosana). The lines inside the plots are linear regression lines generated
using the data set of each plot. (Modified from Chiu et al., 2015)These two characteristics suffering intersexuality are generally found to be sexually dimorphic represent the different roles in the courtship behavior. Female mantids release sex-pheromone to attract the male during the mantid calling behavior
(Robinson and Robinson,1979; Perez, 2005). As a sex-pheromone receptor, the male
mantid typically possesses stronger wings (Robinson and Robinson, 1979; Roy, 2003;Béthoux, 2010; Lombardo and Umbriaco, 2011), and denser grooved basiconic
sensilla, which are hypothesized to be the sensory organ of the sex pheromone (Slifer,1968; Hurd et al., 2004; Holwell et al., 2007; Allen et al., 2012). In H. formosana, the
higher ability of locomotor is not only expressed on the longer wings (Fig. 12), but also the higher ratio of the membranous area in the fore-wing. The fore-wing (tegmen) of a mantids is approximately separated into two parts by the radial vein with the leathery area (AR) above the radial vein for protecting the abdomen and the membranous area (BR) below the radial vein conductive to flying. The wing shape index (BR−AR)/(BR+AR) represents the different ratio of the membranous area to the leathery area while the higher value in the normal male indicates the more membranous wing than that of the female. The wing shape index is changed in the infected male by the decreased value falls between the value of the normal male and the normal female, whereas in the infected female, the shape index is similar to the non-infected one (Fig. 13) (Chiu et al., 2015).Fig. 13. Parasitic effects of the horsehair worm (Chordodes formosanus) on the forewing shapes of infected mantids (Hierodula formosana). (A) The forewing shape index was calculated to determine the difference between the area above (AR) and below (BR) the radial vein. (B) The formula for calculating the forewing shape index is (BR - AR) / (BR + AR). The black solid circles indicate the infected hosts, and the open circles indicate the uninfected hosts.
The large circles surrounding each group (sold line for uninfected hosts, and dashed line for infected hosts) were determined subjectively to approximately include all data points of each group. The four red squares (N: uninfected hosts, IN1–3: infected hosts) in each graph are the trait values corresponding to the pictures of wings on the right side. (Modified from Chiu et al., 2015, the wing vein is referred to Prete et al., 1999)
The antennae in the male H. formosana bear more grooved basiconic sensilla in two ways: the higher density of the sensilla in each flagellum segment
(Fig. 14) and
wider distribution of the sensilla toward to antennal base (Fig. 15A). The grooved basiconic sensilla is distributed in the male H. formosana from the 16th segment (16.42 ± 0.81 (16–18)) to the tip, while that in the female is from the 47th segment (47.10 ± 3.85 (38–55)). In these segments which grooved basiconic sensilla appears in both males and females, the density of the grooved basiconic sensilla is 1.74 to 25 folds in the male. In most of the infected males, both of the density and distribution of the sensilla were changed by the decrease of density in each segment and reduction of the distribution toward the tip of antennae. These two parasitic effects "feminize" the male antennae which makes these two antennal characteristics not significantly different from that of the females. But this does not mean the male antenna is totally feminized. The total number of the flagellum segment, despite it is also sexually dimorphic, in the infected male shows no significant difference to the non-infected ones(Fig. 15B). And again in the female, like the effect in the wing shape, no
parasitic effects on the antennal sensilla were found (Chiu et al., 2015).Fig. 14. Parasitic effect of the horsehair worm (Chordodes formosanus) on the mean (± standard deviation) number of grooved basiconic sensilla per 25 μm2 on 10 selected segments of antennal flagella of infected and uninfected mantid adults (Hierodula formosana). M: uninfected male adult, IM: infected male adult, F: uninfected female adult, IF: infected female adult, NM: last-instar male nymph, NF: last-instar female nymph. (Modified from Chiu et al., 2015)
Fig. 15. Parasitic effect of the horsehair worm (Chordodes formosanus) on the antennal characteristics of the first flagellum segment bearing the grooved basiconic sensilla (A) and the total numbers of flagellum segments (B) of infected and uninfected mantids, Hierodula formosana. Letters indicate significant pairwise differences (multiple comparisons conducted using a Student’s t test with Bonferroni correction, P < 0.05). Statistical analysis of the infected adult males (asterisks) in (A) was performed using the Mann-Whitney
U test because of the violation of normality. (Modified from Chiu et al., 2015)
In summary, the parasitic effect of C. formosanus on H. formosana includes the morphological allometry and intersexuality. The reduced of the wing length has previously been found in the horsehair worm-infected mantids, T. monticola, and suggested as the case of intersexuality (Roy, 2003). Nevertheless, the extreme shorter wings described in Roy (2003) is more likely to be the general parasitic effect which is happened to both sexes of the infected host. In our report in Chiu et al. (2015), the
"real intersexuality" was suggested which the changes are sex dependent instead of that happened on the sex characters. As the morphological changes can be resulted from the developmental manipulation induced by the parasite, the sex dependent change might indicates the different developmental processes undergoing in the opposite sex of the mantids.