Transgenerational Imprints of Sequential Herbivory on Soybean Physiology and Fitness Traits

Sequential herbivory leads to a multitude of effects on plants, influencing processes like growth, physiology, defense, and fitness. However, whether the sequential herbivore attack can elicit any transgenerational consequences is poorly examined. In this study, we show evidence of transgenerational impacts of sequential herbivory by two chewing herbivores, fall armyworm (Spodoptera frugiperda , FAW) and soybean looper (Chrysodeixis includens , SL) on soybean (Glycine max ) progeny. Seeds from the parents subjected to different herbivore sequences (SL-FAW: initial attack by SL followed by FAW and FAW-SL: FAW followed by SL) were used for the transgenerational experiment. Our main hypothesis was that parental sequential herbivory would exert transgenerational effects on progeny traits leading to potential trade-offs. Also, herbivore identity and sequence of attack would critically influence these outcomes. A comprehensive investigation of early growth, physiological performance, physical defense (trichomes) and fitness of the progeny was then carried out. Our results revealed that early growth traits like germination, root morphology, and nitrogen/protein content were similar among maternal treatments; however, significant transgenerational impacts of the sequential attack of SL-FAW were observed in physiological and fitness traits. Notably, no transgenerational effects were observed in physical defenses (trichome density), suggesting an investment in physiology and fitness traits over physical defenses. Collectively, the results confirm that the sequence and identity of herbivore attack in the parental generation can critically shape transgenerational plant responses in soybean, providing novel insights on crop performance under multiple biotic stresses.