Predicting the occurrence of host‐associated differentiation in parasitic arthropods: a quantitative literature review

Abstract

Parasite populations associated with different host species can encounter a variety of isolating reproductive barriers, leading to each population independently accumulating genome-wide genetic differences due to their host associations. This phenomenon is called host-associated differentiation (HAD) and has been proposed as an indicator of early diversification among parasitic arthropods. Although many parasite-host case study systems have been tested for the genetic signature of HAD (e.g., F ST ≥0.15 between sympatric, host-associated populations in the absence of allopatry), it is unknown which isolating reproductive barriers best predict the general occurrence of HAD. HAD development has been attributed to biological and ecological factors that either directly generate reproductive isolation between parasites living on different hosts, such as 'immigrant inviability' (i.e., lower fitness of immigrants in non-native environments), or that promote the accumulation of hostspecific genetic adaptations, such as the gallmaking feeding mode. In fact, some of these factors are shared across multiple case studies, suggesting that the occurrence of HAD is generalizable and can be predicted based on the incidence of significant biological and ecological factors. By means of a discriminant function analysis (DFA), this research assessed 108 arthropod parasite-host case studies for ecological and biological factors significantly correlated with the occurrence of HAD and whether these factors could be used to distinguish the presence of HAD from its absence. The DFA demonstrated that case studies that developed HAD could be distinguished from case studies that did not develop HAD. The results of the DFA were corroborated by a 'non-iterative partial least squares' (NIPALS) discriminant model and a nominal logistic regression. Case studies with HAD could be robustly separated from case studies without HAD based on the incidence of these predictive factors: immigrant inviability, gallmaking, endophagy, recent range invasions of either hosts or parasites, differential host phenology, and differential parasite morphology. These results were used in an infinite random forest analysis to generate a hierarchy of conditional probabilities that separated HAD presence from absence. The results provide researchers with a tool for reliably predicting which untested parasite-host system would likely develop HAD. Immigrant inviability, gallmaking, and their combination were strongly correlated with the presence of HAD, which indicated parasite-host systems with these traits were highly likely to develop HAD. Contrary to expectation, endophagous feeding was negatively correlated with HAD presence, which indicated phytophagous endophagous feeders (excepting gallmakers) were highly unlikely to develop HAD. Furthermore, parasitoids were shown to be just as likely to develop HAD as not. Unfortunately, potentially significant predictive factors (e.g., allochrony) were excluded from analysis because too few case studies have been specifically

Host‐associated genetic differentiation and origin of a recent host shift in the generalist parasitic weed Phelipanche ramosa

“…In the latter case, the divergent selection exerted by the different hosts may result in some genetic divergence among sympatric subpopulations of the parasite, a phenomenon called host‐associated genetic differentiation. Host‐associated genetic differentiation has been well documented, for example, in parasitic arthropods (Harrison et al, 2021 ) and especially in phytophagous insects including agricultural pests (e.g., aphids: Peccoud et al, 2009 ). Parasitic plants have been comparatively much less studied.…”

Effects of genotype and host environment on the cuticular hydrocarbon profiles of Lysiphlebus parasitoids and aggression by aphid-tending ants

“…to mimic host CHC profiles) could plausibly play a role in such specialization, and similar processes have been documented in other chemical mimicry systems [30,31]. Such adaptation could also create barriers to host switching, which is thought to be an important factor in host-associated differentiation in parasitic arthropods [32], although the potential importance of such processes again hinges on whether there is genetic variability in the CHC traits that mediate reduced ant aggression toward Lysiphlebus and on whether the underlying mechanisms are specific to particular aphid hosts. Even if these mechanisms are broadly effective in reducing ant aggression across multiple hosts, however, relevant genetic variation might still enable selection for better specialization to particular aphid species.…”

Fundamental and specialized questions on host race formation and speciation – an introduction

“…Several articles explore the fundamental nature of host race formation itself. In a quantitative assay, Harrison et al (2022) identify just which biological and ecological factors reliably predict the presence of host-associated differentiation for parasitic arthropods. Adaptation to local host plants is key to phytophagous insect speciation, but is geographic variation of a single host plant species enough to cause host race formation?…”