Genetic divergence with ongoing gene flow is maintained by the use of different hosts in phytophagous ladybird beetles genus Henosepilachna

Abstract

Adaptation to different environments can promote population divergence via natural selection even in the presence of gene flow - a phenomenon that typically occurs during ecological speciation. To elucidate how natural selection promotes and maintains population divergence during speciation, we investigated the population genetic structure, degree of gene flow and heterogeneous genomic divergence in three closely related Japanese phytophagous ladybird beetles: Henosepilachna pustulosa, H. niponica and H. yasutomii. These species act as a generalist, a wild thistle (Cirsium spp.) specialist and a blue cohosh (Caulophyllum robustum) specialist, respectively, and their ranges differ accordingly. The two specialist species widely co-occur but are reproductively isolated solely due to their high specialization to a particular host plant. Genomewide amplified fragment-length polymorphism (AFLP) markers and mitochondrial cytochrome c oxidase subunit I (COI) gene sequences demonstrated obvious genomewide divergence associated with both geographic distance and ecological divergence. However, a hybridization assessment for both AFLP loci and the mitochondrial sequences revealed a certain degree of unidirectional gene flow between the two sympatric specialist species. Principal coordinates analysis (PCoA) based on all of the variable AFLP loci demonstrated that there are genetic similarities between populations from adjacent localities irrespective of the species (i.e. host range). However, a further comparative genome scan identified a few fractions of loci representing approximately 1% of all loci as different host-associated outliers. These results suggest that these three species had a complex origin, which could be obscured by current gene flow, and that ecological divergence can be maintained with only a small fraction of the genome is related to different host use even when there is a certain degree of gene flow between sympatric species pairs.

Characterization of ladybird Henosepilachna vigintioctopunctata transcriptomes across various life stages

“…Most Coccinellidae species are beneficial to agriculture, acting as predators of aphids, fungal spores, and moth larvae. However, a few of the Coccinellidae species are pest insects 1 , 3 , eating pollen and even vegetables. Among the pest Coccinellidae species, H. vigintioctopunctata is one of the most destructive pests, causing heavy damage to vegetable crops in some countries, principally those belonging to the Solanaceae family (i.e., Solanum tuberosum , S. melongena , Lycopersicon esculentum , and Lycium spp.).…”

Extremely divergent host plant acceptance with gene flow between sympatric host races of the phytophagous ladybird beetle Henosepilachna diekei

“…; Matsubayashi et al . ). However, we know very little regarding further mechanisms for the removal of genotypes from an alternative host race after hybridization has occurred.…”

“…As the nested model suggests an equally nonzero migration rate between host races (Table S6), ecological and genetic divergence between host races has been maintained even in the face of gene exchange. This pattern, known as "divergence with gene flow" (Rice & Hostert 1993), provides strong evidence for the critical role of natural selection in population divergence against the homogenizing effect of gene exchange between populations (Mallet 2005;Reieseberg 2009;Pinho & Hey 2010;Martin et al 2013;Matsubayashi et al 2017). However, we know very little regarding further mechanisms for the removal of genotypes from an alternative host race after hybridization has occurred.…”

“…Ecologically diverged and partial reproductively isolated populations that inhabit different host plants (“host race” sensu Drés & Mallet ) are suitable materials to elucidate the impact of ecological divergence contributing to reproductive isolation (Berlocher & Feder ; Drés & Mallet ; Matsubayashi et al . , ). The phytophagous ladybird beetle Henosepilachna diekei Jadwiszczak & Wegrzynowicz includes morphologically and ecologically diversified populations depending on various host plant from three families (Acanthaceae, Asteraceae and Lamiaceae) of four genera ( Dicliptera, Mikania, Leucas and Plectranthus ) in South‐East Asia covering Sri Lanka, Thailand, Malaysia and Indonesia (Matsubayashi et al .…”

Host-associated genetic differentiation in the face of ongoing gene flow: ecological speciation in a pathogenic parasite of freshwater fish

“…Our study suggests that the genetic divergence between the two parasite clusters is indicative of speciation with ongoing gene flow, where disruptive selection facilitates reproductive isolation. Direct association between ecological divergence and reproductive isolation is a keenly sought phenomenon in specialist organisms, including parasitic plants (Giraud et al, 2010) phytophagous ladybird beetles (Matsubayashi et al, 2017), parasitic wasps (Stelinski and Liburd, 2005), leaf mites (Skoracka et al, 2013) and phytophagous insects (Berlocher and Feder, 2002; Funk et al, 2002). However, only a few studies explored this link using genomic data and in a framework including ongoing gene flow (Hume et al, 2018; Mateus et al, 2013; Villacis-Perez et al, 2021).…”