A solanum beetle on a fabaceous weed: Host plant generalization and specialization are two sides of the same coin

Investigations of the ongoing evolutionary change of host specificity, especially of that in the initial phase, contribute largely to our understanding of the mechanisms responsible for the diversification of phytophagous insects. However, empirical studies of this aspect in natural systems are very scanty. In the present study, we document the evolutionary change of the degree of adaptation to an introduced legume centro by adults and larvae of the herbivorous ladybird beetle Henosepilachna vigintioctopunctata (Fabricius), which depends normally on various solanaceous plants. Results obtained through experiments conducted in seven successive years revealed a fluctuating degree of adaptation, but with a gradual increase, to centro by H. vigintioctopunctata, showing a tendency towards host plant generalization. Of particular importance, our results suggest that both host plant specialization and generalization are possible evolutionary outcomes of a dynamic initial phase of ongoing host range expansion. In addition, results of quantitative genetic analyses on larval development and other circumstantial evidence suggested that the evolutionary trajectories to specialization/generalization are largely determined by ecological conditions rather than by the insects' intrinsic genetic architecture. We also discuss some special aspects of acquisition of, and adaptation to, novel hosts by H. vigintioctopunctata and other herbivorous beetles, of which adults also feed on plant leaves.     

Adaptive change and conservatism in host specificity in two local populations of the thistle-feeding ladybird beetle Epilachna niponica

We investigated geographic differences in the host specificity of Epilachna niponica Lewis (Coleoptera: Coccinellidae). The Yuwaku population feeds mainly on Cirsium matsumurae Nakai (Asteraceae) and secondarily on Cirsrium kagamontanum Nakai. The Asiu population, located 150 km away from the Yuwaku, feeds exclusively on C. ashiuense Yokoyama et T. Shimizu. Under laboratory conditions, we examined the differences between the two populations in adult feeding acceptance, adult feeding preference, and larval performance, using several closely related thistle species and varieties, including their native hosts. In the Asiu population, adult beetles clearly avoided the host of the Yuwaku population, C. kagamontanum, and no larvae were able to complete their development, whereas in the Yuwaku population, adults accepted and even preferred it to some other thistle species, and about 10% of first instar larvae became adults. This indicates that the Yuwaku population evolved its feeding preference and physiological adaptation to C. kagamontanum through a utilization of this low‐ranked host under natural conditions. Apart from C. kagamontanum, the two populations showed a similar host susceptibility pattern, indicating that this ladybird beetle has a conserved hierarchy in feeding preference and growth performance. We also observed adult leaf choice behavior when given different thistle species, and found that difference in biting rate after palpation determined the leaf areas consumed, implying that factors on the leaf surface played an important role in the choice.     

Asymmetric local adaptation to host plants (Cirsium spp.) by the phytophagous ladybird beetle Henosepilachna niponica and its implications

Divergent host specialization by phytophagous insects is often detected as local adaptation and is thought to have played an important role in their diversification even within an ecological specialist. The phytophagous ladybird beetle Henosepilachna niponica Lewis (Coleoptera: Coccinellidae) predominantly depends on thistles (Cirsium spp., Asteraceae). The distribution of H. niponica occupies multiple areas dominated by different thistle species. This implies the possibility of the occurrence of host-associated divergent specialization of H. niponica. In this study, we investigated the pattern of host-use ability of three allopatric H. niponica populations (Aomori, Iwate, and Yamagata) on three thistle species – Cirsium alpicola Nakai, Cirsium nipponicum (Maxim.) Makino, and Cirsium tonense Nakai – under laboratory conditions. The results displayed asymmetric local adaptation by the beetles. The adults and larvae of the Aomori population showed sufficient acceptance and performance on C. nipponicum and C. tonense, the hosts of the Iwate and Yamagata populations, respectively. On the other hand, the Iwate and Yamagata populations fed small amounts of and performed poorly on C. alpicola, the host of the Aomori population. In contrast, the adults from all the populations clearly preferred feeding on C. nipponicum or C. tonense to C. alpicola. We concluded that the small but significant population differentiation and asymmetric local adaptation by beetles to congeneric host plant species could be a sign of the earliest stage of population divergence by divergent natural selection, given that these divergences will act as ‘immigrant inviability’ and ‘habitat isolation’ at least asymmetrically when these populations come into contact.     

Cryptic local adaptation of the herbivorous ladybird beetle Henosepilachna pustulosa in the ability to use the thistle Cirsium boreale

Local adaptation to different host plants is important in the diversification of phytophagous insects. Thus far, much evidence of the local adaptation of insects with respect to host use at the physiological level has been gathered from systems involving less mobile insects and/or divergent hosts such as plants belonging to different families or genera. On the other hand, the prevalence of such local adaptation of insects with moderate or high dispersal ability to the intraspecific variation of herbaceous hosts is largely unknown. In the present study, we examined the occurrence and degree of local adaptation of the herbivorous ladybird beetle Henosepilachna pustulosa (Kôno) (Coleoptera: Coccinellidae) to its primary host, the thistle Cirsium boreale Kitam. (Asteraceae), through reciprocal laboratory experiments using beetles and thistles from three locations with a range of approximately 200 km. Concerning the larval developmental ability, obvious patterns of local adaptation to the thistles from respective natal locations were detected, at least in some combinations of beetle populations. Similar tendencies were detected concerning adult feeding acceptance, although the statistical support was somewhat obscure. Overall, our results indicate that the degree of local adaptation of insect species with moderate dispersal ability to conspecific herbaceous hosts is occasionally as strong as that involving less mobile insects and/or heterospecific hosts, indicating the potential of such cryptic local adaptation to promote ecological/genetic differentiation of phytophagous insect populations.     

Oviposition site selection by herbivorous beetles: a comparison of two thistle feeders, Cassida rubiginosa and Henosepilachna niponica

In insects that feed on plants in both adult and larval stages, it is often difficult to distinguish oviposition preference from adult feeding preference, because oviposition can occur at or in proximity to feeding sites. In the present study, characteristics of oviposition site selection of two beetle species, Cassida rubiginosa Müller (Coleoptera: Chrysomelidae) and Henosepilachna niponica (Lewis) (Coleoptera: Coccinellidae), were investigated in the field and laboratory, with particular attention to relationships with adult feeding sites. In the field, distances between adult feeding scars and egg masses differed for C . rubiginosa and H . niponica , with the former being very small and the latter averaging 24.6 cm. The same tendencies for the distances between adult feeding scars and egg masses of the two beetle species were confirmed in cages in which only female beetles were released. Cassida rubiginosa restricted egg laying to host plants in the field and to leaves in laboratory assays. On the other hand, H . niponica placed 8% of egg masses on plants adjacent to host plants in the field and often placed eggs on artificial substrates rather than leaf discs in laboratory assays. These results suggest that oviposition and female feeding sites are virtually inseparable in the case of C . rubiginosa , while H . niponica females do not necessarily keep to host plant leaves as oviposition substrates and they tend to oviposit at some distance from their feeding sites. Results are discussed in relation to proximate and ultimate causes of host selection behavior.     

Distribution and host specificity of the thistle‐feeding tortoise beetle Cassida vibex (Coleoptera: Chrysomelidae) in southwestern Hokkaido,northern Japan

The thistle‐feeding tortoise beetle Cassida vibex (Coleoptera: Chrysomelidae) is widespread in the Palearctic region. In Japan, this species has been recorded only from the largest island, Honshu. Here we report the occurrence of this species on Hokkaido, the most northern main island of Japan, along with detailed distributional records from the southwestern part of the island (southern Oshima Peninsula) and information on host plants. We also present the results of laboratory experiments on adult feeding preference and larval developmental performance to determine the specificity of C. vibex for four thistle species (Cirsium grayanum, Cir. alpicola, Cir. yezoense and Cir. aomorense; Asteraceae) common in southwestern Hokkaido. Cassida vibex was detected at only four sites among 97 sites investigated on the Oshima Peninsula, in strong contrast to the common occurrence of the congeneric thistle feeder C. rubiginosa (74 of 97 sites). Cassida vibex was found mainly on Cir. alpicola in the wild, but adult beetles showed no feeding preference for this or three other thistle species when given a choice in the laboratory. Larval performance of C. vibex was similar on Cir. alpicola, Cir. yezoense and Cir. aomorense but significantly lower on Cir. grayanum. Since Cir. alpicola often forms large clumps of individual plants, whereas Cir. yezoense and Cir. aomorense are scattered in their habitats, and C. vibex was collected only at sites where there were dense patches of Cir. alpicola, we postulate that the persistence of C. vibex is possible only where a substantial amount of suitable host plants is available.     

Geographic variation of host use in the leaf beetle Agelasa nigriceps suggests host range expansion

Host range expansion is an important event in the evolution of host use in phytophagous insects. Herein, we report geographic variation of host use in the chrysomelid leaf beetle, Agelasa nigriceps Motschulsky (Coleoptera: Chrysomelidae), and suggest that this beetle is expanding its host range. This beetle has been recently recorded on Pterostyrax hispidus Sieb. et Zucc. (Styracaceae) in addition to its common host plant Actinidia arguta (Sieb. et Zucc.) Planch. ex Miq. (Actinidiaceae). The A. arguta‐associated populations were widely found in Japan, whereas the P. hispidus‐associated populations were found only in central and southwestern Japan. In the present study, we examined adult feeding behavior and larval performance of 12 A. nigriceps populations collected from eight localities, four localities where beetles occurred only on A. arguta (allopatric localities) and four localities where A. arguta‐ and P. hispidus‐associated populations occurred sympatrically (sympatric localities). Beetles of all populations, irrespective of their host plants and localities, showed high acceptance of and high larval performance on A. arguta leaves. In contrast, we found considerable variation in the beetle response to P. hispidus leaves. The A. arguta‐associated populations of allopatric localities scarcely accepted P. hispidus leaves, whereas those of sympatric localities, particularly those of P. hispidus‐associated populations, accepted and grew on P. hispidus leaves, although the degree of acceptance and larval performance varied among localities. These results strongly suggest that A. arguta is the ancestral host for A. nigriceps, and host range expansion to the P. hispidus has occurred in this beetle.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

Oviposition preference of Lycaena salustiusfor,and larval performance on,a novel host plant: an example of ecological fitting

1. ‘Ecological fitting’ is the process whereby the suites of traits an organism carries from previous evolutionary relationships are used to enable colonisation of novel environments or resources. 2. The concept has much explanatory power in studies of novel host associations, particularly when data suggest a deviation from optimal foraging theory, but is often overlooked in studies of herbivore host selection behaviour in favour of evolutionary hypotheses. 3. In the present study, the concept was used to explain the unusual host selection behaviour of the New Zealand endemic oligophagous butterfly Lycaena salustius Fabricius, the larvae of which feed on endemic Polygonaceae species and the introduced and closely related Fagopyrum esculentum Moench. 4. In field cage oviposition choice assays involving only endemic plants, females preferred to oviposit on the rare Muehlenbeckia astonii Petrie. However, the novel host F. esculentum was overwhelmingly preferred in an additional greenhouse assay. In larval no‐choice performance assays, fitness indicators were variable for the novel host. 5. This imperfect relationship between oviposition preference and larval performance is discussed as a possible example of ecological fitting and highlights the potential use of the concept as an explanatory tool in novel host selection behaviour studies.     

Variable correspondence of female host preference and larval performance in a phytophagous ladybird beetle Epilachna pustulosa (Coleoptera: Coccinellidae)

Genetic and environmental factors causing intraspecific variation of the thistle Cirsium kamtschaticum Ledeb. as a host plant of the phytophagous ladybird Epilachna pustulosa Kôno were investigated through simple food-choice tests and rearing of larvae. Two thistle clones (T1U₁ and T4H₂) were used, originally growing approximately 12 km apart. A previous study showed that adult female ladybirds preferred T1U₁ to T4H₂, and that larval performance was better on T1U₁, when leaves from the clones in situ were examined. The two clones retained their characteristics with respect to beetle preference after transplantation into a common garden. However, the difference between T1U₁ and T4H₂ with respect to larval performance was reduced after the transplantation. When leaves from shoots of T1U₁ exposed to different sunlight intensities were offered, adult female ladybirds did not show obvious preferences. Larval eclosion rates increased significantly with the increase in leaf sunlight intensity exposure. These results suggest strongly that both genetic and environmental factors are involved in interclonal variation of thistle quality in beetle preference and/or performance. It is suggested that the quality of thistle leaves for larval performance is largely affected by environmental factors, while leaf quality for beetle preference may be determined strictly by genetic factors. Under certain conditions, E. pustulosa females may behave maladaptively, preferring plants not appropriate for larval growth, or not choosing plants appropriate for the larval growth.