Empirical Evidence of a Bet-Hedging Strategy in the Carrot Cyst Nematode Heterodera carotae

Bet-hedging is an evolutionary strategy encountered in several plant and animal species that allows minimizing the risks by sacrificing mean fitness for a reduction in temporal fitness variation. The objective of the present work was to test the existence of a bet-hedging strategy in plant-parasitic cyst nematodes. The survival stage, the cyst, protects eggs containing second-stage juveniles (J2) and can survive more than ten years in the soil. For some cyst nematode species, hatching of J2 mainly depends on a stimulation by root exudates of their host plant(s). The carrot cyst nematode Heterodera carotae is a good candidate for which a large proportion of juveniles hatch only in the presence of specific chemicals emanating from host roots. Hence, with this narrow host range and facing the impossibility of predicting the presence and quality of host plants, the hypothesis we tested here was that H. carotae should have developed a diversified temporal bet-hedging strategy. Results from in vitro hatching tests demonstrated the existence of a bet-hedging strategy: following a first stimulation by root exudates, the unhatched eggs that remained in the cyst were able to respond to a second stimulation. Moreover, the proportion of J2 hatching at the first or at the second stimulation was strongly impacted by the age of the cyst: older cysts responded better to a first stimulation than young ones. The fitness comparison of both batches of J2 suggested a small fitness advantage for early-hatched juveniles, as they produced 20% more newly formed cysts than late-hatched juveniles. Those results would have applied consequences for the development of a biocontrol strategy that stimulates the hatching of H. carotae juveniles in the absence of its host plant.