Growth–defense trade-offs shape population genetic composition in an iconic forest tree species

Abstract

All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal, Annu. Rev. Plant Biol., 68, 513–534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth–defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipollini et al., Annual Plant Reviews (Wiley, 2014), pp. 263–307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth–defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fast-growing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunner et al., Funct. Ecol. 33, 7–12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.

Plants cultivated for ecosystem restoration can evolve towards a domestication syndrome

“…These increases in size and vigor may appear beneficial at first, as more seeds are available for restoration. However, plant vigor can be selected against in natural populations because of trade-offs between vigor and drought tolerance or herbivory resistance (25)(26)(27). Agricultural cultivation often involves watering and protection from herbivores, which relaxes selection for drought and herbivore resistance, and it may favor high-vigor plants, which produce more seeds and therefore contribute more to the next generation.…”

Effects of condensed tannins on behavior and performance of a specialist aphid on aspen

“…Aspens are long‐lived trees with defence traits that substantially vary with variations in both growth environment (Decker et al, 2017 ) and ontogenetic factors (Cole et al, 2021 ); aspects that have been largely overlooked to date in evolutionary theories of plant defences (Barton & Boege, 2017 ; Hahn et al, 2019 and López‐Goldar et al, 2020 ). Defence response genes in aspen are polymorphic (García & Ingvarsson, 2007 ; Wang et al, 2016a , 2016b , 2020 ) suggestively crafted by extended and complex balancing selective processes (Delph & Kelly, 2013 ; Hurst, 2009 ), and co‐evolution between aphids and their hosts is indeed likely to be an ongoing process that continuously and simultaneously reshapes plants' defensive traits and mechanisms that enable aphids to cope with those traits (Cope et al, 2021 ; Züst & Agrawal, 2016 ). In addition, several piercing‐sucking arthropods live on aspen, including leafhoppers, eriophyid mites, and leaf‐galling aphids of the Pemphiginae (Robinson et al, 2012 ), and resistance might not only protect against piercing damage by one aphid species but against an entire feeding guild as suggested for several plant systems (Kloth et al, 2021 ; Ng & Perry, 2004 ; Nombela et al, 2003 ; von Bargen et al, 2020 ).…”

“…Aspens are long-lived trees with defence traits that substantially vary with variations in both growth environment (Decker et al, 2017) and ontogenetic factors (Cole et al, 2021); aspects that have been largely overlooked to date in evolutionary theories of plant defences (Barton & Boege, 2017;Hahn et al, 2019 andLópez-Goldar et al, 2020). Defence response genes in aspen are polymorphic (García & Ingvarsson, 2007;Wang et al, 2016aWang et al, , 2016bWang et al, , 2020 suggestively crafted by extended and complex balancing selective processes (Delph & Kelly, 2013;Hurst, 2009), and co-evolution between aphids and their hosts is indeed likely to be an ongoing process that continuously and simultaneously reshapes plants' defensive traits and mechanisms that enable aphids to cope with those traits (Cope et al, 2021;Züst & Agrawal, 2016).…”

“…Compounds involved in plants' defences against herbivores and pathogens have well‐established variations with ontogenetic factors (Cope et al, 2021 ) and soil nutrients (Decker et al, 2017 ). Thus, according to recent plant defence theories, potential effects of such factors on plants' resistance must be considered in efforts to elucidate evolutionary interactions between plants and consumers (Barton & Boege, 2017 ; Hahn et al, 2019 ).…”

“…Aspens are deciduous, early succession trees that are widely distributed in forests of the Northern hemisphere (Rogers et al, 2019 ). Aspen trees have also been used as models in studies of intraspecific differences in defence chemistry (Häikiö et al, 2009 ; Hartikainen et al, 2009 ; Keefover‐Ring et al, 2014 ; Lindroth & Hwang, 1996 ; Rubert‐Nason & Lindroth, 2021 ), inter‐ and intraspecific variation in defence genes (Bernhardsson et al, 2013 ; Wang et al, 2016a , 2016b , 2020 ), environmental modulation of metabolic priorities (Bandau et al, 2015 , 2021 ; Cole et al, 2021 ; Cope et al, 2021 ; Decker et al, 2017 ; Dettlaff et al, 2018 ; Gaur et al, 2022 ), and molecular mechanisms involved in induced defence responses (Barbehenn & Peter Constabel, 2011 ; Barrios‐San Martín et al, 2014 ; Ramírez et al, 2004 ; Ullah et al, 2018 , 2019 ). They are also regarded as strong foundation species in temperate and boreal forests (Cole et al, 2021 ), hosting genotype‐specific communities of arthropods (Barker et al, 2019 ; Robinson et al, 2012 ), and pathogens (Albrectsen et al, 2010 ; Bandau et al, 2015 ; von Bargen et al, 2020 ).…”