Insect-Plant Interactions •  Phytophagous insects account for approximately 40% of all described

insects. In 1964 Paul Ehrlich and Peter Raven published a paper that argued that the incredible proliferation of phytophagous insects and higher plants is the result of a coevolutionary process between them. According to this scenario the evolution of terrestrial plants presented a new adaptive zone for insects to exploit. As insects evolved means to exploit plants as food, plants evolved countermeasures which led to greater diversification of plants and further diversification of insects. Increased diversification of plants also led to increased structural diversity in habitats, and increased diversification of phytophagous insects led to increased diversification at higher trophic levels. Thus much of present day diversity on earth may be the result of evolutionary interactions between insects and plants.

•  In an earlier lecture we examined the physiological adaptations of insects for feeding on plants protected by toxic secondary compounds. In today's lecture we will explore some of the more long-term aspects of coevolution between plants and insects. First we will ask whether in fact phytophagy was an evolutionary innovation that led to increased diversification of insects. And then we will examine the evidence for coevolution between insects and plants.

Coevolution and Adaptive Radiation Coevolution is the evolution of characteristics of two or more species in response to changes in each other. Coevolution occurs when two or more species produce reciprocal changes in one another. It has two components:

1. Coadaptation is the degree of mutual modification between lineages. It can be expressed as gene for gene changes in two lineages or in a more diffuse way, involving many genes. Coadaptation represents the microevolutionary aspects of coevolution.

2. Cospeciation is the degree of mutual phylogenetic association between two lineages. It is said to occur when the phylogenies of two lineages are concordant. Cospeciation represents the macroevolutionary aspect of coevolution.

Adaptive radiation is the evolution of a variety of forms from a single ancestral stock, often after colonizing an island group or entering a new adaptive zone. This may include speciation, but not necessarily.

Adaptive Radiation of Phytophagous Insects A major tenet of the Ehrlich & Raven hypothesis is that plants initially represented a new, unexploited adaptive zone for insects. Insect that successfully colonized this adaptive zone then underwent an adaptive radiation, leading to enhanced diversification. Can this tenet be tested? To test the adaptive-zone hypothesis we must asked whether adaptive shifts are repeatedly associated with accelerated diversification across many independent groups. Is the phytophagous habit associated with accelerated diversification in insects? How do we compare diversification rates among lineages? Sister-group analysis is one approach.

Sister Group Analysis of Adaptation

•  By definition, sister groups are the same age.

•  Any differences in diversity between sister groups reflect different rates of diversification.

•  An adaptive shift occurs when a lineage moves from an ancestral adaptive zone to a new one. The hypothesis of adaptive radiation is supported if the sister group that has undergone the adaptive shift is consistently more diverse than the sister group that remains in the ancestral adaptive zone.

•  The statistical power of sister-group analysis is increased when a particular adaptive shift occurs in many independent groups.

Test of the phytophagous insect diversification hypothesis

•  Higher-plant feeding is found in 9 orders of insects. It has probably arisen at least 50 times in just the extant forms with known habits.

•  Present phylogenetic information allows the identification of 13 pairs of sister groups, one of which feeds on higher plants and the other of which does not.

•  In 11 of these 13 sister-group pairs, the phytophagous lineage is more diverse than its presumed non-phytophagous sister group. Thus the phytophagous feeding habit is associated with increased diversification. This provides tentative support of the Ehrlich & Raven hypothesis.

Diversification of plants in response to feeding by phyotophagous insects

•  As phytophagous insects diversified on plants, plants should respond by escalating their defenses against insects.

•  Resin and latex canals found in many plants presumably serve as a defense against plant-feeding insects.

•  Are plants with resin and latex canales more species rich compared to their sister groups?

•  In 13 out of 16 groups the answer is yes.

Scenarios for the evolution of insect-plant associations

•  Concordant cladogenesis (association by descent).

•  Discordant cladogenesis (insect colonization of pre-existing plants; resource tracking).

•  Concordant cladogenesis due to homoplasy or convergent evolution of secondary plant compounds.

•  Partial concordant.

Example of Concordant Cladogenesis

•  In 14 phylogenetic analyses, only 1 showed extensive concordance, 3 showed partial con-cordance and 10 showed no concordance.

•  Phyllobrotica on Scutellaria in the Lamiaceae (mint family). Strong evidence of cospeciation.

Example of Discordant Cladogenesis

•  Ophraella on Asteraceae (sunflower family). Little evidence of cospeciation.

•  Differences in the degree of phylogenetic concordance in these groups may reflect the relative strength of constraints operating in the two systems. Phyllobrotica depends on its host plant throughout all life stages (adults use host-plant compounds for defense against predators), whereas Ophraella does not.

•  Although strict, prolonged, pairwise cospeciation b/w insects and plants is rare, they have experienced a long history of coadaptation.