Effective specialist or jack of all trades? Experimental evolution of a crop pest in fluctuating and stable environments

Abstract

Understanding pest evolution in agricultural systems is crucial for developing effective and innovative pest control strategies. Types of cultivation, such as crop monocultures versus polycultures or crop rotation, may act as a selective pressure on pests' capability to exploit the host's resources. In this study, we examined the herbivorous mite Aceria tosichella (commonly known as wheat curl mite), a widespread wheat pest, to understand how fluctuating versus stable environments influence its niche breadth and ability to utilize different host plant species. We subjected a wheat-bred mite population to replicated experimental evolution in a single-host environment (either wheat or barley), or in an alternation between these two plant species every three mite generations. Next, we tested the fitness of these evolving populations on wheat, barley, and on two other plant species not encountered during experimental evolution, namely rye and smooth brome. Our results revealed that the niche breadth of A. tosichella evolved in response to the level of environmental variability. The fluctuating environment expanded the niche breadth by increasing the mite's ability to utilize different plant species, including novel ones. Such an environment may thus promote flexible host-use generalist phenotypes. However, the niche expansion resulted in some costs expressed as reduced performances on both wheat and barley as compared to specialists. Stable host environments led to specialized phenotypes. The population that evolved in a constant environment consisting of barley increased its fitness on barley without the cost of utilizing wheat. However, the population evolving on wheat did not significantly increase its fitness on wheat, but decreased its performance on barley. Altogether, our results indicated that, depending on the degree of environmental heterogeneity, agricultural systems create different conditions that influence pests' niche breadth evolution, which may in turn affect the ability of pests to persist in such systems.

Understanding the joint evolution of dispersal and host specialisation using phytophagous arthropods as a model group

“…The presence of genetic variation can also be inferred from experimental evolution responses. Numerous studies using this methodology have documented the rapid evolution of host range (Sousa et al ., 2019; Mortier & Bonte, 2020; Laska et al ., 2021; Olazcuaga et al ., 2021; Skoracka et al ., 2022) and dispersal (Belliure, Montserrat & Magalhães, 2010; Bitume et al ., 2011; Fronhofer et al ., 2014; De Roissart et al ., 2016; Lustenhouwer et al ., 2023) in herbivores. Such responses imply that sufficient genetic variation for these traits is present in the original population.…”

“…Therefore, the role of temporal host variability in selecting for specialists or generalists in plant–herbivore systems in the field remains in need of study, in part because it is difficult to establish the true host range of herbivores in temporally variable landscapes (Laska et al ., 2021). Studies on experimental evolution have shown that temporal variation affects different life‐history traits in herbivores (Magalhães et al ., 2014; De Roissart et al ., 2016) including dispersal (Fronhofer et al ., 2014) and host range (Skoracka et al ., 2022). However, studies measuring both traits are lacking.…”

Editorial: Regulation of proteolysis and proteome composition in plant response to environmental stress

“…They must cope with miscellaneous abiotic stresses usually enhanced by heavy industry ( Labudda et al., 2022 ). Moreover, changes in climate conditions and agricultural systems are favourable to pests and pathogens gradation on plants ( Nykiel et al., 2022 ; Skoracka et al., 2022 ). However, plants are not defenceless; they are equipped with a battery of multiple mechanisms (from molecular through biochemical-physiological to structural) that are activated by them to ensure further growth and development and the production of diasporas ( Muszyńska and Labudda, 2019 ; Formela-Luboińska et al., 2020 ; Tokarz et al., 2020 ; Tokarz et al., 2021 ; Fidler et al., 2022 ; Miernicka et al., 2022 ).…”

Life-history adaptation under climate warming magnifies the agricultural footprint of a cosmopolitan insect pest

“…Such responses are energetically costly and therefore need to be compensated by either increased resource intake 5,19 , or by diverting resources away from reproduction in favour of cellular maintenance 20,31 . Such alternative strategies in pest species' life-history are predicted to impact both their invasion potential and the footprint left on their hosts 1,14,17,[32][33][34] , and thus, can have important consequences for pest management 1,3,35 .…”