Stagewise resolution of temperature-dependent embryonic and postembryonic development in the cowpea seed beetle Callosobruchus maculatus (F.)

Abstract

Background The thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to temperature, including changes in the thermal thresholds and thermal sensitivity during early development. Even postembryonic development of many cryptically living species is understood superficially at best. Results This study is the first to estimate the exact durations of developmental stages in the cowpea seed beetle C. maculatus from oviposition to adult emergence at five permissive constant temperatures from 20 to 32 °C. Early embryonic development was tracked and documented by means of destructive sampling and subsequent confocal imaging of fluorescently stained specimens. Late embryonic and early larval development was studied with the use of destructive sampling and light microscopy. Well-resolved temporal series based on thousands of embryos allowed precise timing of the following developmental events: formation of the blastoderm; formation, elongation, and retraction of the germ band; dorsal closure; the onset and completion of sclerotization of the cuticle; hatching, and penetration of the first-instar larva into the cowpea seed. Pupation and adult eclosion were observed directly through an incision in the seed coat. The thermal phenotype of C. maculatus was found to vary in the course of ontogeny and different stages scaled disproportionately with temperature, but pitfalls and caveats associated with analyses of relative durations of individual stages are also briefly discussed. Conclusion Disproportionate changes in developmental durations with temperature may have important implications when study design requires a high degree of synchronization among experimental embryos or when the occurrence of particular stages in the field is of interest, as well as in any other cases when development times need to be estimated with precision. This work provides one of the first examples of integration of embryological techniques with ecophysiological concepts and will hopefully motivate similar projects in the future. While experiments with Drosophila continue to be the main source of information on animal development, knowledge on other model species is instrumental to building a broader picture of developmental phenomena.

Annual variability in the sound acorn production of Quercus serrata is regulated by a seed‐predatory weevil in western Japan

“…In addition, we observed that, in captivity, M. ursulus tends to suffer earlier mortality when smaller acorns are provided as a food source from late June to early July (K. Hirayama and K. Mizo, personal observation). Kutcherov (2020) reported that larval and pupal developmental rates significantly increased with temperature in the cowpea seed beetle Callosobruchus maculatus . Based on these observations, we assumed that higher temperatures in June would probably promote the earlier emergence of M. ursulus adults, which may thereby lead to a phenological mismatch between their sap‐sucking behavior and the growth of Q. serrata acorns.…”

Cold plasma disinfestation of Callosobruchus maculatus infested soybeans: Its subsequent impact on soymilk extraction yield and quality

“…Hence, it was found that the egg samples treated after 15-18 h (after it was laid/oviposition) were more sensitive to CP treatment than the other two samples. Since eggs will be in two nuclei stages with a wet outer layer between 0 and3 h after oviposition (Kutcherov, 2020), they showed better resistance to CP treatment as compared to eggs that were in the process of developing embryo (15-18 h old) (de Sá et al, 2014). In contrast, the eggs that were more than 36 h old have shown more resistance to CP treatment as the embryogenesis process already produced an embryo inside the eggs.…”

Variation in thermal sensitivity of diapause development among individuals and over time predicts life history timing in a univoltine insect

“…For example, genetic variation within populations can explain a substantial portion of interindividual variation in development duration that is often observed even under highly controlled laboratory conditions (Kingsolver et al 2004). In addition, different life history stages (earlier vs. later in ontogeny) can exhibit different relationships between temperature and development rate that may be incorporated into predictive models (Yurk and Powell 2010; Lopatina et al 2014; Sinclair et al 2016; Kutcherov 2020). As with any thermal performance curve, the thermal maximum, the maximal performance value, or curve breadth may vary among individuals and across ontogeny.…”

“…Just as thermal sensitivity may vary among individuals and over time during morphogenic development (Yurk and Powell 2010; Lopatina et al 2014; Sinclair et al 2016; Kutcherov 2020), diapause development performance curves may differ among individuals and over time. For example, early diapause (e.g., initiation, maintenance) may have a different thermal sensitivity than late diapause (e.g., termination), which we have not captured in our simple models (Fig.…”

“…Ontogenetic variation in thermal sensitivity of development is another important source of variation in development times/rates that is well described and often incorporated into predictive models (Yurk and Powell 2010;Lopatina et al 2014;Sinclair et al 2016;Kutcherov 2020).…”