A Northward Habitat Expansion Along With Directional Gene Flow in Two Microscopic Herbivores

Speciation is frequently accompanied by gene flow, a phenomenon that is recognised as ubiquitous in nature. However, the role of gene flow in speciation remains unclear, particularly in tiny and sympatric arthropods that lack clear geographic isolations. This study aims to uncover how sympatry, parapatry and allopatry underlie the speciation process in two monophagous mites, Epitrimerus sabinae and Glossilus juniperensis, which belong to the E. sabinae complex and infest coniferous plant (Juniperus chinensis). We conducted whole-genome resequencing of 298 mite individuals from 56 populations, spanning nearly 20 years of field surveys, to determine the drivers shaping species distribution patterns and to explore the role of gene flow in speciation. Population structure analyses revealed four genetic groups, corresponding to allopatric southern G. juniperensis and northern E. sabinae, and sympatric central G. juniperensis and central E. sabinae; the sympatric E. sabinae and G. juniperensis populations were linked by sharing mixed ancestry. Our demographic history analyses showed that these two species derived from an ancestral lineage in southern China and diverged in the late Pleistocene, followed by a northward expansion along with varied degrees of gene flow. The genetic differentiation of both species was positively affected by geographic distance and environmental factors. Our results reveal a pattern of speciation in two mite species, initiated by genetic divergence with gene exchange between two species (sympatry) and followed by genetic isolation and habitat expansion (parapatry or allopatry). Our findings underscore a one-way-northward-habitat expansion along with directional gene flow in two herbivores speciation.