Kei W. Matsubayashi

Ecological speciation in phytophagous insects

Divergent natural selection has been shown to promote speciation in a wide range of taxa. For example, adaptation to different ecological environments, via divergent selection, can result in the evolution of reproductive incompatibility between populations. Phytophagous insects have been at the forefront of these investigations of ‘ecological speciation’ and it is clear that adaptation to different host plants can promote insect speciation. However, much remains unknown. For example, there is abundant variability in the extent to which divergent selection promotes speciation, the sources of divergent selection, the types of reproductive barriers involved, and the genetic basis of divergent adaptation. We review these factors here. Several findings emerge, including the observation that although numerous different sources of divergent selection and reproductive isolation can be involved in insect speciation, their order of evolution and relative importance are poorly understood. Another finding is that the genetic basis of host preference and performance can involve loci of major effect and opposing dominance, factors which might facilitate speciation in the face of gene flow. In addition, we raise a number of other recent issues relating to phytophagous insect speciation, such as alternatives to ecological speciation, the geography of speciation, and the molecular signatures of speciation. Throughout, we aim to both synthesize what is known, as well as highlight areas where future work is especially needed.

Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F1 hybrid inviability, and sexual selection against F1 hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.

Matriphagy in the hump earwig, Anechura harmandi (Dermaptera: Forficulidae), increases the survival rates of the offspring

Females of the hump earwig, Anechura harmandi, are completely consumed by their offspring at the end of their care (matriphagy). The effect of this matriphagy was assessed by manipulative experiments. Matriphagy led to a delay in the dispersal of the nymphs and an increase in their survival rate. The same results were obtained when mothers were removed and the nymphs were given sufficient food. Females separated from their offspring after larval hatching failed to produce a second clutch, and three-quarters of them did not develop their ovaries. These results suggest that the survival of nymphs and their stay in the nest are dependent on food availability and that A. harmandi females are strictly semelparous.

Distribution and Differentiation of Henosepilachna diekei (Coleoptera: Coccinellidae) on Two Host-Plant Species Across Java, Indonesia

ABSTRACT Divergent natural selection on different host plants may be a crucial factor in promoting the remarkable diversity of phytophagous insects, and might occur in any geographical context. Because the intensity and consequences of divergent selection on different hosts can vary depending on the degree of gene flow between conspecific insect populations, elucidating the geographical context and degree of host specificity in the incipient phase of differential host use is indispensable to understanding the diversification process in phytophagous insects. Henosepilachna diekei Jadwiszczak & Węgrzynowicz (Coleoptera: Coccinellidae) is a tropical ladybird beetle occurring mainly on two host species from different plant families, Asteraceae and Lamiaceae. We investigated the geographical distribution of H. diekei across Java, Indonesia, in relation to the availability of the two hosts, and examined the host specificity of beetles in the laboratory. We also investigated genetic relationships among local populations of beetles using mitochondrial NADH dehydrogenase subunit 2 gene sequences. Geographic variation in host use by H. diekei was largely determined by skewed geographical distributions of the hosts, although there was a synergistic effect with extremely divergent host specificity by the beetles. The molecular analyses suggested that genetic differentiation among the beetle populations has occurred and has been maintained by the effects of both geographical distance and divergent host specificity. The geographical distribution of H. diekei populations differing in host specificity suggests that geographical distance, local host-plant availability, and divergent host specificity contribute synergistically to promote the genetic differentiation and subsequent diversification of phytophagous insects on different hosts.

Genome size increase in the phytophagous ladybird beetle Henosepilachna vigintioctomaculata species complex (Coleoptera: Coccinellidae)

This study reports genome size (C‐value) estimates for seven species of ladybird beetles (Coleoptera: Coccinellidae) in Japan using flow cytometry. The results demonstrated genome sizes of 1.0–1.4 Gb in four closely related phytophagous ladybird beetles belonging to the Henosepilachna vigintioctomaculata species complex. These values were approximately two times larger than that of a congeneric phytophagous ladybird beetle H. vigintioctopunctata (0.66 Gb), and of two very distantly related common carnivorous ladybird beetles, Harmonia axyridis (0.46 Gb) and Coccinella septempunctata (0.42 Gb). These lines of evidence suggest that rapid and large genome size increase occurred just after the branching of the common ancestor of the H. vigintioctomaculata species complex from other ladybird species.

Differential acceptance of and survivorship on a non- host plant between two geographically separate populations of the phytophagous ladybird beetle Henosepilachna yasutomii

Phytophagous specialists among insects occasionally accept plants they do not or only rarely utilize under natural conditions. This non‐host acceptance could represent an initial stage in host‐range evolution. Here, we examined adult acceptance of and larval survivorship on a non‐host plant – wild thistle, Cirsium kamtschaticum Ledeb. (Asteraceae) – for two geographically separate populations of the phytophagous ladybird beetle Henosepilachna yasutomii Katakura (Coleoptera: Coccinellidae), which normally utilizes blue cohosh, Caulophyllum robustum Maxim. (Berberidaceae), in the wild. The two beetle populations showed lower acceptance of and survivorship on the non‐host plant (thistle) than on the normal host plant (blue cohosh). Furthermore, they differed significantly in their responses to thistle but not to blue cohosh. Even for the beetle population that more readily accepted thistle as adults, acceptance was moderate and the eclosion rate was low, indicating reduced performance on the non‐host plant. Although studies have infrequently focused on non‐host acceptance, this is likely common in phytophagous specialists and thus is a potentially important evolutionary factor, as it may determine the future direction of food‐range evolution.

Introgression and Habitat Segregation in a Pair of Ladybird Beetle Species in the Genus Propylea (Coccinellidae, Coccinellinae) in Northern Japan

The ladybird beetles Propylea quatuordecimpunctata and P. japonica have largely overlapping distributions in northern Japan, and in the laboratory produce fertile hybrids. In this study, we surveyed the distribution and morphological differentiation of these species and the hybrids in natural populations, with a focus on western Hokkaido, northern Japan. Phenotypic analyses were conducted for 987 individuals collected at 90 localities. In addition, the nuclear internal transcribed spacer-II (ITS2) region (549 bp) and part of the mitochondrial cytochrome c oxidase subunit I (COI) gene (700 bp) were sequenced for 620 individuals from 53 localities. Analyses of both phenotypic and genotypic features discriminated two distinct entities assignable to P. quatuordecimpunctata and P. japonica. However, individuals with intermediate phenotypes and/or genotypes also occurred extensively, indicating natural hybridization. Putative P. quatuordecimpunctata individuals were collected across a wide range of altitudes (30–600 m), whereas those of P. japonica were found mostly lower than 300 m alt. In addition, P. quatuordecimpunctata was dominant in semi-open habitats shaded by canopy foliage, whereas P. japonica was frequent in more open habitats. The perceived altitudinal difference in the distributions may thus in part be a consequence of this different habitat preference, as open habitats are more common at lower altitudes in the study area.