Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies

Abstract

A central but little-tested prediction of ''escape and radiation'' coevolution is that colonization of novel, chemically defended host plant clades accelerates insect herbivore diversification. That theory, in turn, exemplifies one side of a broader debate about the relative influence on clade dynamics of intrinsic (biotic) vs. extrinsic (physical-environmental) forces. Here, we use a fossil-calibrated molecular chronogram to compare the effects of a major biotic factor (repeated shift to a chemically divergent host plant clade) and a major abiotic factor (global climate change) on the macroevolutionary dynamics of a large Cenozoic radiation of phytophagous insects, the leaf-mining fly genus Phytomyza (Diptera: Agromyzidae). We find one of the first statistically supported examples of consistently elevated net diversification accompanying shift to new plant clades. In contrast, we detect no significant direct effect on diversification of major global climate events in the early and late Oligocene. The broader paleoclimatic context strongly suggests, however, that climate change has at times had a strong indirect influence through its effect on the biotic environment. Repeated rapid Miocene radiation of these flies on temperate herbaceous asterids closely corresponds to the dramatic, climatedriven expansion of seasonal, open habitats.adaptive radiation ͉ coevolution ͉ climate change ͉ macroevolution ͉ Agromyzidae

Macroevolution and the biological diversity of plants and herbivores

“…In perhaps the most convincing example, Wheat et al (72) ascribe the radiation of the butterfly subfamily Pierinae, which is much more diverse than its sister group, to the evolution of a nitrile-specifier protein that detoxifies the glucosinolate defenses of their diverse Brassicales hosts. In this Special Feature, Winkler et al (92), in a new phylogenetic analysis, provide evidence that evolutionary shifts to chemically different plant clades are associated with elevated diversification in leafmining flies.…”

Distinguishing Agromyzidae (Diptera) Leaf Mines in the Fossil Record: New Taxa from the Paleogene of North America and Germany and Their Evolutionary Implications

“…The assignment was based on the distinctive, intermittent fluidized frass trail, which distinguishes them from other fossil leaf mines, most lepidopterous in origin, studied by these authors. Winkler et al (2009b) examined the same material and briefly proposed other characteristics that, considered together, allow confident attribution of these trace fossils specifically to Agromyzidae. These characters, discussed in more detail above, include alternation of the frass trail at the sides of the mine for some portion of the mine.…”

“…Wilf et al (2006) reported agromyzid leaf mines from the early Paleocene of southeastern Montana, USA, and we consider these to be the oldest known record of Agromyzidae. These locally abundant fossils were briefly characterized and figured by Wilf et al (2006), and more recently by Winkler et al (2009b), who used them to calibrate a time scale of agromyzid evolution.…”

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants

“…This long history of interaction, coupled with negative effects of herbivores on plant fitness [5], are credited with promoting the macroevolutionary diversification of defensive traits and elevating speciation rates in plants [3,6]. In turn, diversification of plant defences and species has promoted the diversification and specialization of herbivores [7,8]. Thus, plant -insect coevolution is thought to have given rise to much of the macroscopic diversity of life on the Earth [3,9,10].…”