Explaining the occurrence of host-associated differentiation: A quantitative literature review.

Authors: Harrison, Kyle; TARONE, AARON - Texas A&M University; DEWITT, THOMAS - Texas A&M University; MEDINA, RAUL - Texas A&M University

Submitted to: Entomologia Experimentalis et Applicata
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/18/2021
Publication Date: N/A
Citation: N/A

Interpretive Summary: Parasites can evolve into reproductively isolated, genetically distinct populations by associating with different host species. This type of evolution is called host-associated differentiation (HAD) and is potentially responsible for the diversity observed among parasitic arthropods. The accumulation of HAD case studies has lead to the proposal of many possible factors that explain the occurrence of HAD (i.e., factors that can result in ecological or reproductive isolation). However, the relative abundance of these factors among HAD case studies has yet to be formally tested. The authors performed a quantitative study of the HAD literature to establish an overarching pattern of correlation between potentially explanatory factors and HAD occurrence. A discriminant analysis of HAD occurrence established a hierarchy of HAD likelihood based on explanatory factors. The authors discovered that the incidence of immigrant inviability, gall-making, and their combination best explain the presence of HAD in a given parasite-host system. Also, contrary to expectation, endophagous feeding best explains the absence of HAD, indicating that endophagous insects are not expected to experience HAD.

Technical Abstract: Background: When reproductive isolation evolves between parasite populations living on different host species, each population can independently accumulate genome-wide genetic differentiation due to their host-specific associations. This phenomenon is called host-associated differentiation (HAD) and has been proposed as the origin of the biodiversity observed in parasitic arthropods. Although many parasite-host case study systems have been shown to involve HAD, it is uncertain which ecological and biological traits best explain the general occurrence of HAD. Still, several factors have been proposed within verbal models aimed to explain the evolution of HAD in specific case study systems. The proposed factors that best explain the occurrence of HAD involve mechanisms that facilitate reproductive isolation among parasites on different host species (e.g., endophagy, asexual reproduction, or allochrony). However, these factors have yet to be quantitatively correlated with the presence of HAD. In this study, we performed a quantitative literature review that evaluated the correlation between potential explanatory factors and the general occurrence of HAD. Results: A discriminant analysis of HAD occurrence based on the incidence of explanatory factors demonstrated that parasite-host case study systems involving HAD can successfully be distinguished from case studies without HAD. Based on this, an infinite random forest analysis was used to generate a hierarchy of conditional probabilities based on the incidence of significant explanatory factors. The hierarchy of factor-based conditional probabilities provides a tool for making reliable predictions about the likelihood of a given parasite-host system to show HAD and indicates distinct routes toward its acquisition. Conclusion: We discovered that the incidence of immigrant inviability, gall-making, and their combination best explain the presence of HAD in a given parasite-host system. Also, contrary to expectation, endophagous feeding best explains the absence of HAD, indicating that the majority of endophagous feeders are not expected to experience HAD.