Pollination impacts how plants respond to herbivore attack

A new study pub­lished in Evol­u­tion Let­ters shows that when plants evolve under dif­fer­ent pol­lin­a­tion regimes, their responses to herb­ivory also dif­fer. Flori­an P Schi­estl tells us more.

What hap­pens when a herb­i­vore starts feed­ing on a plant? Most often, plants respond by upreg­u­lat­ing their defense mech­an­isms, such as increas­ing their tox­icity or pro­du­cing more defens­ive hairs. Inter­est­ingly, such improved defense often comes at the cost of decreased flower dis­play, such as flower size or volat­ile sig­nal­ing, and, as a con­sequence, reduced pol­lin­at­or attractiveness.

Tra­di­tion­ally, such plas­ti­city after herb­i­vore attack is thought to have evolved through selec­tion imposed by herb­i­vores. If herb­i­vores invari­ably attack plants for many gen­er­a­tions, gen­o­types with con­stant high defenses enjoy an advant­age, because they don’t lose time with upreg­u­lat­ing defenses while herb­i­vore slowly des­troy them. As a con­sequence, non-plastic, high defense gen­o­types become more com­mon and plastic gen­o­types decrease in the pop­u­la­tion. In pop­u­la­tions where herb­i­vores attack vari­ably and “unpre­dict­ably”, the oppos­ite scen­ario will take place, and plants with plastic defenses will be favored, because defense is costly and they can use their resources more effi­ciently, for example by invest­ing in pol­lin­at­or attrac­tion and seed production. 

In our recent paper in Evol­u­tion Let­ters we show that along­side herb­i­vores, pol­lin­at­ors also strongly influ­ence the evol­u­tion of herb­i­vore-induced plas­ti­city. We used plants ori­gin­at­ing from an exper­i­ment­al evol­u­tion study, where they evolved for six gen­er­a­tions with or without con­stant (pre­dict­able) herb­ivory, and with either hand pol­lin­a­tion or bumble­bee pol­lin­a­tion. These plants were infes­ted with herb­i­vores and then their induced responses meas­ured. Inter­est­ingly and unex­pec­tedly, the presence/absence of bumble­bees had the strongest effects on herb­i­vore-induced responses of sev­er­al traits, both for defense traits (tox­ic com­pounds) as well as for flor­al traits. Over­all, plants with bumble­bee pol­lin­a­tion had more plastic traits and showed stronger responses to herb­ivory than those with hand pollination. 

A plant (Brassica rapa) being sim­ul­tan­eously vis­ited by a pol­lin­at­or (Bom­bus ter­restris) and eaten by a herb­i­vore (Peiris brassicae).

We also found an asso­ci­ation between trait val­ues and their plas­ti­city, such that for traits that increased after herb­ivory (defense traits), high trait val­ues ten­ded to be asso­ci­ated with lower plas­ti­city, and for traits that decreased after herb­ivory (mostly flor­al traits), high trait val­ues were asso­ci­ated with high­er plas­ti­city. This res­ult points towards a meta­bol­ic trade-off between the evol­u­tion of traits and their plas­ti­city. When plants evolve high defenses, they are not able to upreg­u­late them a lot any­more. On the oth­er hand, those plant indi­vidu­als with large flowers and strong scent emis­sion, also suf­fer most under down-reg­u­la­tion of these traits as a side-effect of herbivory. 

These res­ults show how defense and pol­lin­a­tion are linked in many ways in plants: first, through the meta­bol­ic costs of either pro­du­cing defense com­pound or attract­ive flowers, and secondly through the evol­u­tion­ary link of pol­lin­at­or-favored flor­al traits and herb­i­vore-induced plas­ti­city in defense.

Pro­fess­or Flori­an P Schi­estl is based at the Depart­ment of Sys­tem­at­ic & Evol­u­tion­ary Bot­any, Uni­ver­sity of Zürich, Switzer­land. The ori­gin­al art­icle is freely avail­able to read and down­load from Evol­u­tion Letters.