Transovum Transmission of Trypanosomatid Cysts in the Milkweed Bug, Oncopeltus fasciatus

Abstract

Leptomonas wallacei is a trypanosomatid that develops promastigotes and cystic forms in the gut of the hemipteran insect Oncopeltus fasciatus. Insect trypanosomatids are thought to be solely transmitted from one host to another through the ingestion of parasite-contaminated feces. However, here we show that L. wallacei cysts present on the eggshells of eggs laid by O. fasciatus can also act as infective forms that are transmitted to the insect offspring. Newly hatched O. faciatus nymphs are parasite-free, but some of them become contaminated with L. wallacei after feeding on eggshell remnants. The present study is the first report of transovum transmission of a trypanosomatid, a process that may have a relevant role in parasite’s within-host population dynamics.

Symbiont transmission entails the risk of parasite infection

“…Collectively, such findings demonstrate that L. pyrrhocoris is transmitted across host generations in a manner that is identical to the beneficial Coriobacteriaceae symbionts [7]: vertically via the egg surface and horizontally through contact with infected firebugs, specifically their faeces ( figure 2a,b). This is consistent with recent findings in milkweed bugs and their trypanosomatid parasite, Leptomonas wallacei [13], where transovum propagation of the parasite was demonstrated to mediate vertical transmission. Despite the parallels to the transmission cycle of L. pyrrhocoris, it is unclear whether the egg probing behaviour in Oncopeltus fasciatus is relevant for symbiont transmission, considering the lack of evidence for vertically transmitted mutualists associated with milkweed bugs [14].…”

Obligate development of Blastocrithidia papi (Trypanosomatidae) in the Malpighian tubules of Pyrrhocoris apterus (Hemiptera) and coordination of host-parasite life cycles

“…It encompasses the members of two formal genera still to be revised: Blastocrithidia and polyphyletic Leptomonas (only species related to Leptomonas jaculum ). These flagellates are distinct from others in their ability to form a specialized resting stage–cyst-like amastigotes (CLAs), adapted to long-term survival in the environment [ 12 – 14 ]. All species of this group known to date were described from true bugs (order Hemiptera) [ 2 , 11 , 15 , 16 ].…”

“…However, there are some exceptions: Blastocrithidia triatomae parasitizing triatomine bugs, Leptomonas wallacei from the lygaeid bug Oncopeltus fasciatus , and B . papi from the firebug Pyrrhocoris apterus [ 12 , 15 , 31 ]. Blastocrithidia triatomae was extensively studied because of its pathogenic effect on the insect hosts, which transmit Chagas disease [ 31 , 32 ].…”

“…Leptomonas wallacei inhabits the host's midgut and hindgut, forming CLAs in the host rectum. The parasite is transmitted horizontally by coprophagy or vertically via eggs’ surface contamination [ 12 ]. The most recently described species, B .…”

Trypanosomatids Detected in the Invasive Avian Parasite Philornis downsi (Diptera: Muscidae) in the Galapagos Islands

“…Infected insect hosts include species in the orders of Diptera, Hymenoptera, Siphonaptera, Hemiptera, and Lepidoptera, among others [ 22 , 23 ]. Trypanosomatids can be transmitted vertically or horizontally between insects [ 24 , 25 , 26 , 27 , 28 ], and are easily transferred via ingestion of infected fecal matter from other insects and other food sources [ 24 , 29 ]. Infections with trypanosomatid parasites in insects have a wide range of pathogenicity and virulence, from unnoticeable effects on their hosts to decreased energy levels, lower fitness, negative immune system effects, and sometimes death [ 29 , 30 , 31 , 32 , 33 , 34 ].…”