To protect against herbivores that constantly attack them, plants have evolved defenses that have direct detrimental effects on herbivores affecting their movement, growth, development, feeding, oviposition (Kessler and Baldwin, 2001; Rostás et al., 2003). Plants also harm herbivores indirectly by attracting their natural enemies such as predators and parasitoids (Gols et al., 2008). Both direct and indirect defenses can be constitutive and/or induced (Karban et al., 1997). Constitutive defenses are present regardless of herbivory pressure and consist of surface wax, cuticle, trichomes, and other physical barriers or chemical defenses which deter the establishment of insect pests or affects its growth and development (Gatehouse, 2002). On the other hand, induced defenses are activated as the response to pest attack, which can enhance the plant resistance to the further attack of that insect pest and/or for pests possessing different feeding guilds (Karban and Myers, 1989). Physical defenses, also called structural or mechanical defenses, are the structural modifications that plants possess to deter herbivory. These are also the first line of defense owned by plants which comprise spines, thorns, trichomes and plant waxes. Spines are sharply pointed modified petioles, midribs, veins or/and stipules and provide protection to the plants against herbivory (Hanley et al., 2007; Kariyat et al., 2017). Trichomes are the hair like protuberances from different parts of the plants. These have defensive function against herbivory by acting as a physical barrier, impeding insect movement, delaying or/and deterring herbivore feeding and oviposition, thus making them exposed longer and vulnerable to its predators (Levin, 1973; Dalin et al., 2008; Peiffer et al., 2009; Kaur J. and Kariyat R. R., 2020). Chemical defenses are chemical compounds which are stored in the plant tissues (constitutive) or induced in response to herbivory (induced; Ryan, 1990; Turlings and Benrey, 1998; Sun et al., 2019). These include but are not limited to volatile organic compounds, salicylic, ethylene and jasmonate pathways and various other primary and secondary metabolites including antibiotics, alkaloids, and terpenes, to name a few (Ryan, 1990; Kessler and Baldwin, 2001; Rivard et al., 2004; Howe and Jander, 2008; Degenhardt et al., 2010; Singh et al., 2021). Besides constitutive and induced defenses of plants, tri-trophic interactions of host plants with parasitoids and predators of herbivores also provides them with an additional line of defense. Sometimes the feeding damage done by herbivores to host plants invites herbivore’s natural enemies. Plants release volatiles to attract natural enemies such as predatory mite, Phytoseiulus persimilis (Mesostigmata: Phytoseiidae) as seen in case of tomato plants, Solanum esculentum (Solanaceae) when they are fed by two-spotted spider mite, Tetranychus urticae (Trombidiformes: Tetranychidae; Kennedy, 2003).

Although plants have evolved an astonishing variety of defenses that include physical and chemical defenses, that could be constitutive or induced. Insect herbivores still feed extensively on plants causing continuous damage affecting their fitness. Over a long period of evolutionary history, insect herbivores have evolved a wide array of traits including modifications to their feeding habits and mouth parts. Additionally, to continue their predatory relationship with plants, they also possess elaborate mechanisms and behavioral modifications to avoid, process, sequester, or excrete plant defenses and defensive compounds allowing them to initiate feeding. For instance, herbivores such as caterpillars and beetles having chewing and biting type mouth parts feed on leaves and cause significant photosynthetic tissue loss (Rowell and Simpson, 1992; Wise, 2007). Sucking and piercing type herbivores such as true bugs and aphids. Feeding by sucking and piercing type herbivores such as true bugs and aphids, not only lead to loss of photosynthates from vascular tissues, but also transmit viral diseases (Wisler et al., 2007; Ishikawa and Takahata, 2019). The tiger wing butterfly, Mechanitis isthmia (Lepidoptera: Nymphalidae) have the cooperative feeding and webbing behavior on solanaceous plants covered with dense trichomes as a behavioral adaptation to evade defenses. The young larvae of these butterflies shave the trichomes to feed on leaf tissues and construct silken webs to avoid their piercing by trichomes (Young and Moffett, 1979). Tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae) feeding on tobacco, Nicotiana spp. (Solanaceae) is adapted to feed and efficiently excrete nicotine, a pyridine alkaloid possessing insecticide properties. Monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae) is adapted to feed on, sequester and use toxic cardenolides in milkweed, Asclepias sp. (Apocynaceae) to protect itself against predators (Malcolm, 1994). For more specific details on Solanum herbivores and their feeding habits, see Supplementary Table 1.

Since plant defenses are costly (Baldwin, 1998; Kariyat et al., 2013; Yip et al., 2019; Garcia et al., 2021) taking up already limited resources originally allocated for their growth and reproduction, plants are found to exhibit trade-offs for growth, reproduction, and defense traits (Bazzaz et al., 1987; Kariyat et al., 2013). In general, available plant resources and their sources, i.e., leaves and roots determine the plant growth, commonly measured as the biomass gain over time. This gain in biomass is the result of conversion of primary metabolites into cellular building blocks (Shih, 2018). Where herbivory has a quantifiable negative impact, it leads to the redirection of this energy and matter from growth to defense traits and hence the trade-offs for growth and reproduction comes into play. For natural and unmanaged systems, in which the cost of defense has major effects on the evolutionary trajectory of the species, these trade-offs can have both short- and long-term effects on fitness. However, one of the true measures of plant fitness—the number of successful offspring it can produce in future generations is difficult to measure in such systems, when compared to the agro-ecosystems, where seed set or general plant growth/ biomass can be used as a measure of its fitness and thus, easier to measure (Stireman et al., 2005). To understand the mechanisms governing plant defense trade-offs in both natural and managed ecosystems, with both pairwise and multi-trophic interactions involving biotic and abiotic factors, various hypotheses and theories have been put forward and tested. In this review, we revisit some of the major theories and use Solanum genus as a model to explain the assumptions and trade-off traits, providing suggestions for additional lines of inquiries.

Solanaceae is a diverse plant family consisting of ~90 genera and ~2,700 species which are found in all habitats ranging from dry deserts to wet tropical rainforest and have growth habits ranging from small ephemeral herbs to large perennial trees (Gebhardt, 2016). Among all the genera in Solanaceae, Solanum genus contributes for over 1,500 species in the family (Tchatchouang et al., 2017). This diverse group can be a good study model as it contains economically important food crops such as potato (Solanum tuberosum), eggplant (S. melongena) and cultivated tomato (S. lycopersicum); drug plants including bittersweet nightshade (S. dulcamara), dutch eggplant (S. aculeatissimum) and New Zealand eggplant (S. aviculare); ecologically important weeds including horsenettle (S. carolinense), silverleaf nightshade (S. elaeagnifolium), earleaf nightshade (S. mauritianum), black nightshade (S. nigrum) and American black nightshade (S. americanum); annuals including hairy nightshade (S. sarrachoides) and west Indian nightshade (S. ptychanthum); perennials including horsenettle (S. carolinense) and silverleaf nightshade (S. elaeagnifolium); self-compatible species including pepino (S. muricatum), hairy nightshade (S. villosum); self-incompatible including the ornamental nightshade (S. bulbocastanum) and jasmine nightshade (S. jasminoides; Symon, 1981; Rushing et al., 1985; Blackshaw, 1991; Hermanutz and Weaver, 1996), and species with plasticity in self-incompatibility (S. carolinense, S. elaeagnifolium; Kariyat et al., 2012a). In addition to this, sequenced genomes of species such as tomato (S. lycopersicum) and potato (S. tuberosum; The Potato Genome Sequencing Consortium, 2011; The Tomato Genome Consortium, 2012) makes the genus amenable for genome wide molecular work for conspecifics (Kariyat et al., 2012b).

The high species count, and a wide range of growth habits have led the genus Solanum to evolve tremendous variation in defense traits. The species in the Solanum genus have both constitutive and induced, physical and chemical defenses against herbivory that show variation both inter and intraspecifically, with consequences for trophic interactions. Structural defenses in Solanum mainly consist of trichomes, spines and waxes. An enormous variation in morphology, types, density and dimensions have been reported for trichomes of Solanum (Anjana et al., 2008; Howe and Jander, 2008; Kim et al., 2012; Cho et al., 2017; Kariyat et al., 2018; Watts and Kariyat, 2021a, 2022), with variation for density and types on abaxial and adaxial surfaces, with functional consequences for herbivores (Malakar and Tingey, 2000; Horgan et al., 2007; Kariyat et al., 2013; Kaur I. and Kariyat R. R., 2020; Watts and Kariyat, 2021b), a similar trend of interspecific variation and anti-herbivore defenses functions have also been found for spines (Kariyat et al., 2017), and epicuticular wax (Watts and Kariyat, 2022). Moving past the structural defense barrier in Solanum, the herbivores are then exposed to a gamut of chemical defenses starting from the leaf surface messengers, Ca²⁺ and Reactive Oxygen Species (ROS). For example., study in tomato have demonstrated that, the oral secretions of tobacco hornworm caterpillars induce ROS, which are then suppressed in the presence of a Ca²⁺ chelator, suggesting herbivore-associated elicitor induced signaling pathway (Gandhi et al., 2020; further reviewed in detail in Gandhi et al., 2021). Along with oral secretions, excreta or oviposition fluids are also known to act as chemical cues perceived by transmembrane pore proteins in Solanum (Gandhi et al., 2021). More interestingly, the plants of Solanum carolinense has shown trade-offs between constitutive and induced defenses (Kariyat et al., 2013) where the insect suppression reduced the induced resistance significantly more than the constitutive defenses (Coverdale and Agrawal, 2022). The intraspecific variation in Solanum genus also can also lead to differential chemical defense induction (Campbell et al., 2013; Calf et al., 2018; Müller et al., 2020) in herbivores with similar feeding habits. Tomato plants when fed by the corn worm, Helicoverpa zea (Lepidoptera: Noctuidae) altered more metabolites than feeding by tobacco hornworm, and that includes defense related metabolites such as phenolics and precursors of amino acids (Steinbrenner et al., 2011). Also, the alteration and reallocation of primary metabolites and the differential induction of metabolites in different leaves have been documented where tomato plants when damaged by tobacco cutworm, Spodoptera litura (Lepidoptera: Noctuidae) resulted into reallocation of primary metabolites like sugars and amino acids from local to systemic leaves. Differential defense related response was observed as local leaves increased lignin accumulation, and systemic leaves had significant induction of secondary metabolites including chlorogenic acid, caffeic acid and catechin (Kundu et al., 2018). While hormonal signaling pathways and the gene networks (Kariyat et al., 2012b) that mediate them warrants a stand-alone review, in a nutshell—the phytohormone Jasmonic acid is found to play a very important role in plant defense against herbivores (Howe and Jander, 2008). When chewing herbivores damage plants, it leads to activation of Jasmonic acid signaling pathway that leads to both direct toxin induction and also indirect defenses through the induced emission of various herbivore induced plant volatiles (HIPV’s), which can act as antifeedants and also as cues for predators or parasitoids (Kariyat et al., 2012a,b). These defensive volatiles can be produced either locally or systemically and can be flavonoids, terpenoids and alkaloids (Wasternack and Parthier, 1997). For example, on attack by Tuta absoluta, the tomato plants emit volatiles, induced by jasmonic acid which as a result attracts mirid predators (Silva et al., 2018). To mitigate the omnipresent impact of herbivory, plants use trade-offs, and in Solanum, the trade-offs vary by species, breeding status and genetic variation of plants (inbred vs. outbred, maternal families), plant characteristics, herbivore, and environmental conditions as well.

Taken together, we have innumerable studies of plant defenses (Wilkens et al., 1996; Lawrence et al., 2008; Alba et al., 2009; Horgan et al., 2009; Kaplan et al., 2009; Rodríguez-López et al., 2011; Tian et al., 2014; Kundu et al., 2018; Kariyat et al., 2012a,b, 2017, 2018, 2019; Taher et al., 2019; Kaur I. and Kariyat R. R., 2020; Kaur J. and Kariyat R. R., 2020) and trade-offs (Wise and Sacchi, 1996; Cipollini et al., 2004; Walls et al., 2005; Wise et al., 2008; Underwood and Halpern, 2012; Kariyat et al., 2012a,b, 2013) possessed by Solanum plants in case of their interactions with herbivores. However, how defenses and trade-offs function simultaneously in plants to ward-off herbivores has not been recently discussed at length. To address this, in this review, we used Solanum genus as a model to re-explore trade-offs for defenses by plants infested by herbivores varying in their feeding habits and specialization on host plants.

As discussed in this review, plant growth defense trade-offs are well illustrated by the diverse members of Solanum genus defending against even more diverse community of insect herbivores (Supplementary Tables 1, 2). There is always a balance that plants strike between growth and defense, governed by maintenance of optimal fitness. There is a wide array of plant defense mechanisms against the herbivores belonging to different types of feeding guilds (Supplementary Table 1), and hence the trade-offs associated with them are also very diverse. The chewing type herbivores induce JA pathways and other related defenses (Figure 1; Redman et al., 2001), but the sap sucking herbivores are known to induce SA pathway defenses (Figure 1; Tan and Liu, 2014). Owing to the active research on the costs of plant defenses, our understanding of the mechanisms governing these trade-offs has been enhanced in past few decades. However, our knowledge is still scant on the economics of cost vs. quality in terms of defense and growth, and there are several issues which still need to be addressed.

Most of the hypotheses have not been tested vigorously. Realistically, testing of proposed hypotheses directly and including all components of the hypothesis is near to impossible (Stamp, 2004). Assuming that testing is possible, whole setup required for testing hypotheses required intensive amount of work, place, labor, money etc., to list a few factors which limits the studies and rigorous testing of hypotheses. Another major issue with some hypotheses is the lack of proper definition/equation for different factors being used in defining the hypothesis (Smilanich et al., 2016). For example, some of the constraints in plant apparency hypothesis include: how to differentiate between a specialist and a generalist herbivore? What exactly apparency is? How can it be measured? In most of the studies which tested some hypotheses, a pairwise comparison has been done using a couple of plant species or in contrasting climatic conditions, however whether the same results apply to other systems is not definite (Pavia et al., 2002). Furthermore, some results are justified partially with one hypothesis and partially with the other hypothesis (Heckman, 2011). Some hypotheses apply only to a certain sub-category of plant-insect interaction niche, as seen in case of apparency hypotheses, which focus primarily on comparing defenses of perennial plants/trees with annuals. Although trade-offs deal with costs of fitness, measuring the costs of fitness directly is difficult especially in case of optimal defense hypothesis and thus, can lead to completely different results for experiments performed by two different scientists. In numerous extreme cases, the hypothesis completely fails to explain the defense-growth pattern in plants when attacked by herbivores (Barto and Cipollini, 2005; Heckman, 2011; Hattas et al., 2017). Additionally, none of the studies that we found have investigated trade-offs in case of co-infestation or sequential infection by two or more herbivores.

There is no hypothesis which has been accepted universally so far and is perfect and all of them has their own flaws and contradictions. Scientists over decades suggested amendments to the hypothesis based on different systems and results obtained over the years. These amendments occasionally work and obtained results match the predictions (López-Goldar et al., 2020). Despite the changes, some hypotheses have completely been rejected do its utmost failure, other have been partially accepted with a hope of improvement and some have been widely accepted. For example, Plant apparency hypothesis and carbon nutrient balance hypothesis have been almost completely rejected, growth-differential balance hypothesis and optimal defense hypothesis have been partially accepted, and resource availability has been the most accepted hypothesis as it justifies most of the studies, their predictions and obtained results. And thus, it has been adopted the most and considered to be the best hypotheses to explain defense-fitness-trade-offs in plants.

One of the solutions for several of the above-mentioned issues is to consider pros and cons of these hypotheses and to come up with an integrated hypothesis/equation which can make predictions for defense-fitness-trade-offs in plants with minimum errors and deviations. This hypothesis can then be tested in different systems to validate it over the years. Solanum genus can prove to be perfect for testing proposed/existing hypotheses. Solanum is found in all kinds of habitats and climatic conditions. Most studies tested theories in a chosen climate because of prevalence of the focus plant species in that area. However, with Solanum, because of its ubiquitous prevalence around the globe, comparative studies in different climatic conditions such as dry areas and wetlands can be done. Plethora of insect species with different feeding habits are found on Solanum plants (Supplementary Tables 1–3). Those insects damage different plant parts which makes it easier to test plant response in case damage done by chewing type herbivore and sucking type herbivore. For example, M. sexta feeds primarily on leaves of Solanum, but grubs of Synanthedon rileyana feed primarily on roots (Supplementary Table 1). Thus, studies contrasting growth-defense trade-offs in above-ground and underground plant parts can be done. Solanum genus contains self-pollinated, cross-pollinated, self-compatible and self-incompatible plants, using which study of trade-offs can be expanded in look into phylogenetic trade-offs pattern development across the genus. Solanum genus consisting of tomato, potato and eggplants is already a study model in many labs focusing on different aspects of insect-plant ecology. Most of Solanum species are easy to grow and maintain in controlled conditions. Solanum plants are both annuals and perennials, so theories which require a longer project time such as apparency theory and resource availability theory can also be tested using this genus. Numerous studies have already done been done on Solanum genus as model or/and because of economic value of the focus plant species. Available data and knowledge from those studies makes it easier to quantify genus specific multiple physical and chemical traits for testing defense-fitness-trade-off hypotheses. Overall, Solanum possess numerous properties which can make it a model for testing and studying plant defense-fitness-trade-offs and fill up the knowledge gap discussed in text above.

RK, SW, and SK conceived the idea. SW and SK wrote the first draft. All authors contributed to the article and approved the submitted version.

This project was supported by Presidential Graduate Fellowship to SW from University of Texas Rio Grande Valley. The publishing was supported by the Open Access Publishing Fund administered through the University of Arkansas Libraries.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.