Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae)

Abstract

Resource sharing within clonal plant networks can occur via the translocation of water, nutrients, and photoassimilates through rhizomes and stolons. Similar mechanisms may mediate the sharing of information (e.g., about herbivory or other environmental stressors) among ramets via molecular or biochemical signals. The storage of such information in belowground structures could facilitate the transmission of appropriate phenotypic responses across growing seasons in perennial species. However, few previous studies have explored the potential transfer of ecologically relevant information within such networks. This study addresses the effects of foliar herbivory and belowground overwintering on the growth and flowering, physical defenses, and herbivore resistance in the clonally spreading species Solanum carolinense L. (Solanaceae). We used rhizomes from inbred and outbred plants that were repeatedly exposed to feeding damage by Manduca sexta L. (Sphingidae) caterpillars and rhizomes from undamaged control plants. These rhizomes were either planted immediately or exposed to overwintering conditions and allowed to produce new ramets (rhizomatous offshoots). We then assessed offshoot emergence, flowering, physical defense traits, and herbivore performance. Relative to controls, offshoots of herbivore-damaged plants exhibited greater spine and trichome densities, and reduced performance of M. sexta larvae. However, they also emerged and flowered significantly later, and produced fewer flowers than offshoots of undamaged plants. Inbreeding also negatively affected offshoot emergence, flowering, trichome production, and herbivore resistance. These effects of parental herbivory were more pronounced in outbred offshoots, indicating that inbreeding may compromise the trans-seasonal induction of plant defenses. Finally, exposure to overwintering conditions increased trichome production and reduced caterpillar performance on offshoots. Together, these results show that induced defenses can be transmitted through rhizomes and affect offshoot growth, flowering, defensive traits, and herbivore resistance. They also document fitness-related costs associated with defense induction in offshoots and suggest that the transfer of defenses across seasons can be compromised by inbreeding.

Transgenerational impacts of herbivory and inbreeding on reproductive output in Solanum carolinense

“…Insect herbivory can have severe negative effects on plant growth, development, and reproduction (Crawley, 1989(Crawley, , 1992(Crawley, , 1997Louda, 1989;Gange, 1990;Marquis, 1992;Strauss and Zangrel, 2002). Some of these fitness-related costs are due to direct predation of plant reproductive structures (Janzen, 1971;Crawley, 1992;Louda and Potvin, 1995;McCall and Irwin, 2006;González-Megías, 2016), while others are associated with trade-offs that result in the reallocation of resources away from plant growth and reproduction and toward either compensation for lost leaf material or the induction of anti-herbivore defenses (Herms, 1992;Trumble et al, 1993;Cipollini et al, 2003;Huot et al, 2014;Züst and Agrawal, 2017;Nihranz et al, 2019). For example, chewing insect herbivores can induce plant defenses that directly interfere with herbivore feeding (e.g., spines, trichomes, secondary metabolites) and indirect defenses that attract natural enemies of the herbivores (e.g., volatile organic compounds) (De Moraes et al, 1998;Paré and Tumlinson, 1999;Kessler and Baldwin, 2002;Holeski, 2007;Kariyat et al, 2013;Barton, 2015).…”

Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense

“…carolinense , inbreeding adversely affects both physical and chemical defenses [ 10 , 38 , 40 , 46 ], resulting in greater amounts of herbivore damage under field conditions [ 43 , 44 , 54 ], increased oviposition by M . sexta adults [ 87 ], reduced recruitment of herbivore natural enemies upon herbivore attack [ 46 ], and lower induction of anti-herbivore defenses [ 10 , 11 , 34 ]. Here, we show that the adverse effects of maternal inbreeding on plant defenses extend to the outbred offspring of inbred plants.…”

“…While the mechanisms of transgenerational effects of herbivory are not fully understood, they may be caused by maternally derived epigenetic modifications of the offspring genome and/or movement of herbivore-induced hormones or small molecular RNAs from maternal tissue to developing seeds [ 31 , 32 ]. Notably, transgenerational induced anti-herbivore defenses could benefit plant offspring in environments with high herbivore pressure but may adversely affect reproductive output in environments with low herbivore pressure [ 11 ].…”

Efficiency of using electric toothbrush as an alternative to a tuning fork for artificial buzz pollination is independent of instrument buzzing frequency

“…The Solanaceae plant family is a model for studying SI and the species that exhibit it tend to be obligate outcrossers, and in some cases, SI breaks down with floral age [13] leading to selfing, and consequently inbreeding depression, [21] which plays a significant role in the evolution of mating systems [22]. Most studies on inbreeding and/or genetic variation and their effects on fitness traits require pollen extractions, pollen trait measurements, and controlled pollinations [23]. In the case of tomatoes and other economically important crops, breeding programs also require the use of such methods for pollen extraction and subsequent selection studies.…”