2. Biology of Ixodiphagus spp. and Geographic Distribution
Information on the biology of
Ixodiphagus species is insufficient and mainly limited to experimental studies
[10]. The entire life cycle ranges from 28 to 70 days, and starts when female wasps lay eggs into ticks through the penetration of their ovipositor into the tick’s body (
Figure 1). After hatching, larvae (
Figure 2) develop inside the tick. While no information is available about the pupal stage, adult wasps emerge from their tick hosts through a hole at the posterior end, with mating occurring soon after the emergence
[9]. There have been no studies assessing the number of
Ixodiphagus eggs released by females in natural conditions. However, based on experimental studies, it is estimated that during the entire life span,
I. hookeri and
I. texanus lay about 120 and 200 eggs, respectively
[23,24][13][14].
Figure 1.
Life cycle of
Ixodiphagus
spp.
Figure 2.
Ixodiphagus
sp. larva in a
Rhipicephalus sanguineus
s.l. tick (Scale bar = 200 μm).
Information about the preference for certain tick developmental stage remains unclear. For instance, some
resea
uthorchers reported that larvae of
Ixodiphagus are mostly detected in tick nymphs and adults when the latter are engorged, suggesting that parasitism is likely to occur in blood-fed ticks rather than in unfed ones
[25][15]. However, an experimental study demonstrated that unfed nymphs of
I. ricinus were more parasitized than other stages
[10]. This observation was later confirmed with the finding of
I. hookeri DNA in unfed
I. ricinus nymphs collected from the environment
[3]. Furthermore, it has been demonstrated that unfed ticks can be collected from vegetation, and after feeding them on laboratory animals (e.g., mice) the parasitoids emerge
[26][16]. In their searching for ticks,
Ixodiphagus spp. females may be driven by chemical attractants produced by vertebrate animals hosting ticks
[10], as well as by tick feces
[27][17]. In fact, some experiments have demonstrated that
I. hookeri females appear to be attracted by odors produced by the haircoat of roe deer (
Capreolus capreolus) and wild boar (
Sus scrofa)
[10] but not from those of mice, cattle, and rabbits
[10]. This mechanism of attraction is crucial for facilitating the encounter of
Ixodiphagus spp. with their preferred tick species
[8], increasing the chances of completion of their lifecycle. Despite this observation, this is most likely not the general scenario in nature. It is believed that in most cases, hosts are attractive for ticks, in which eggs of the parasitoids are already present. The development of wasp larvae is directly dependent on nutrients contained in the engorged blood meal of the ticks; hence it is unlikely that
Ixodiphagus larvae could develop in unfed ticks due to the depletion of nutrients
[28][18]. This translates into a correlation between the occurrence of
Ixodiphagus larvae, tick density, and infestation rate in vertebrate hosts
[8,29][8][19]. For example, in
I. scapularis nymphs the infestation of wasp parasitoids occurred only in individuals parasitizing white-tailed deer (
Odocoileus virginianus) in the northeastern USA, and in areas with deer population density of 13–20 animals per km
2 or higher
[29][19]. In addition, no association was observed between the occurrence of wasps and
I. ricinus infesting rodents in northern Europe
[8], suggesting that the species of vertebrate host is crucial for the behavior of
Ixodiphagus spp.. Despite the lack of an association between wasps and ticks of rodents, it is known that in laboratory conditions parasitoids develop and emerge from ticks that feed on mice. The dynamic of
Ixodiphagus has been poorly assessed in field conditions. Based on the few studies conducted so far, adults fly for a short period of time. In Germany, adult wasps were found during 3–5 weeks, in late summer/early fall
[10]. This seasonal activity overlaps with a high density and feeding activity of
I. ricinus immature stages in the same area, which incidentally occurs when vertebrate hosts are also more abundant. For example, it has been demonstrated that wasps from ticks fed before July have a shorter developmental time compared with those from ticks engorged later on
[10]. This finding is similar to those previously observed in field conditions in Texas (USA), where wasps required a development time of 25 and 33 days for ticks fed in May and September, respectively
[9].
In southern Italy, the majority of ticks that tested positive for
I. hookeri (i.e., 92%) were collected during fall–winter (from October to March)
[3], when
I. ricinus peaked
[30][20]. Overall, the detection in ticks is related to developmental time of
Ixodiphagus and to the synchronization with tick development
[10]. Curiously, non-embryonated eggs of
I. hookeri are able to survive over winter inside unfed nymphs of
I. ricinus [31][21] and
I. scapularis [6,25][6][15]. From a biological perspective, this characteristic allows wasp populations to survive through different seasons in spite of unfavorable climate conditions (e.g., extreme cold).
The molecular detection of
Wolbachia endosymbionts in
I. hookeri [32][22] suggests that it could be the reason for the presence of
Wolbachia pipientis in
I. ricinus [33][23], with a role in their parthenogenesis (i.e., development from unfertilized eggs). This is demonstrated in other hymenopteran species (e.g.,
Encarsia pergandiella)
[34][24]. Despite the suggested parthenogenesis for
Ixodiphagus [24][14], the potential involvement of
Wolbachia has never been demonstrated. Recently, the assessment of the microbiota in
I. ricinus in high-throughput sequencing revealed the presence of a wide plethora of microorganisms, including
I. hookeri and
Wolbachia [35][25]. These multiple interactions among microorganisms in
I. ricinus may affect a wasp population, influencing differences in its biology observed in different tick populations worldwide
[10,36,37][10][26][27].
Ixodiphagus spp. have been widely reported in various species of ixodid ticks, with a broad distribution across all five inhabited continents
[4[4][28][29],
38,39], but more commonly reported from Europe and the US
[3,6,29][3][6][19]. In fact, several hard tick species within the genera
Amblyomma,
Dermacentor,
Haemaphysalis,
Hyalomma,
Ixodes, and
Rhipicephalus, in various life stages, have been found parasitized by
Ixodiphagus wasps (
Table 1). So far, the only argasid soft tick found parasitized by an
Ixodiphagus species (
I. mysorensis) was
Ornithodoros sp.
[40][30].
Table 1.
Distribution of
Ixodiphagus
spp. parasitizing different tick species in the world.
Parasitoid |
Tick |
Tick Life Stage |
Country |
Reference |
I. texanus |
H. leporispalustris |
Nymph |
United States |
[2] |
I. hookeri |
R. sanguineus |
Nymph |
United States |
[41][31] |
I. hookeri |
R. sanguineus, D. marginatus |
Nymph |
United States |
[9] |
I. hookeri |
I. ricinus |
Nymph |
France |
[42][32] |
I. hookeri |
H. concinna, D. reticulatus, D. venustus, R. sanguineus |
NA |
France |
[43][33] |
I. hookeri |
R. sanguineus |
Nymph |
Brazil |
[44][34] |
I. hookeri |
R. sanguineus |
NA |
India |
[45][35] |
I. hookeri |
D. nitens |
NA |
United States |
[46][36] |
I. hookeri |
D. variabilis |
NA |
United States |
[11] |
I. hookeri |
H. aegyptium |
NA |
South Africa |
[47][37] |
I. hookeri |
R. sanguineus |
Nymph |
Nigeria |
[48][38] |
I. hookeri |
I. cookei |
Nymph |
United States |
[49][39] |
I. hookeri |
R. sanguineus |
NA |
United States |
[50][40] |
I. texanus |
H. leporispalustris |
Nymph |
United States |
[51][41] |
I. hookeri |
R. sanguineus |
Nymph |
United States |
[52][42] |
I. mysorensis |
Ornithodorus sp. |
NA |
India |
[40][30] |
I. texanus |
I. persulcatus |
Nymph |
Russia |
[53][43] |
I. hookeri |
I. ricinus |
Nymph |
Czech Republic/Slovakia (Czechoslovakia) |
[54][44] |
I. hookeri |
R. sanguineus |
Nymph |
Kenya |
[55][45] |
I. hookeri |
R. sanguineus |
Nymph |
Africa |
[56][46] |
Ixodiphagus sp. |
H. bancrofti, H. bremneri, I. holocyclus, I. tasmani |
NA |
Australia |
[57][47] |
I. hookeri |
R. sanguineus |
NA |
Indonesia |
[58][48] |
I. hookeri |
R. sanguineus |
Nymph |
Malaysia |
[59][49] |
I. texanus |
H. leporispalustris |
Larva, Nymph |
Canada |
[60][50] |
I. hookeri |
I. dammini |
Nymph |
United States |
[21][51] |
I. hookeri |
H. punctata |
Nymph |
Spain |
[61][52] |
I. hookeri |
A. variegatum |
Nymph |
Kenya |
[62][53] |
I. hookeri |
I. ricinus |
NA |
France |
[63][54] |
I. texanus |
I. dammini |
Nymph |
United States |
[64][55] |
I. hookeri |
R. sanguineus |
Nymph |
Mexico |
[65][56] |
I. hookeri |
I. scapularis |
Nymph |
United States |
[66][57] |
I. hookeri |
I. scapularis |
Nymph |
United States |
[25][15] |
I. hookeri |
A. variegatum |
Nymph |
Kenya |
[67][58] |
I. hookeri |
I. scapularis |
Nymph |
United States |
[29][19] |
I. hookeri |
R. sanguineus |
Nymph |
Venezuela |
[68][59] |
I. hookeri |
A. variegatum |
Nymph |
Kenya |
[37][27] |
I.hookeri |
H. concinna |
Nymph |
Slovakia |
[26][16] |
I. taiaroaensis |
I. uriae, I. eudyptidis |
Larva, Nymph |
New Zealand |
[69][60] |
I. hookeri |
I. ricinus |
Nymph |
Germany |
[10] |
I. hookeri |
I. ricinus |
Nymph |
Netherlands |
[32][22] |
I. hookeri, I. texanus |
R. sanguineus, Amblyomma sp. |
Nymph |
Brazil |
[70][61] |
I. hookeri |
I. ricinus |
Nymph |
France |
[32][22] |
I. hookeri, I. texanus |
R. sanguineus |
Nymph |
Panama |
[71][62] |
I. hookeri |
I. ricinus |
Nymph, Adult |
Italy |
[3] |
I. hookeri |
I. ricinus |
Nymph |
Slovakia |
[22][63] |
Ixodiphagus sp. |
R. sanguineus |
Nymph, Adult |
Brazil |
[4] |
I. hookeri |
I. ricinus |
Nymph |
Finland |
[5] |
I. hookeri |
R. sanguineus |
Nymph |
United States |
[72][64] |
I. hookeri |
R. microplus, I. persulcatus, D. silvarum, H. concinna |
Adult |
Côte d’Ivoire, Senegal, Russia |
[39][29] |
I. hookeri |
I. ricinus |
Larva, Nymph |
Netherlands |
[8] |
I. hookeri |
I. ricinus, H. concinna |
Nymph |
Slovakia |
[1] |
I. hookeri |
I. ricinus |
Nymph |
France |
[35][25] |
I. hookeri |
I. ricinus |
Nymph |
United Kingdom |
[73][65] |
I. hookeri |
A. nodosum |
Nymph, Adult |
Brazil |
[74][66] |
I. hookeri |
I. ricinus |
Nymph |
Hungary |
[6] |