Ecology and Evolution of Gall-Inducing Arthropods: The Pattern From the Terrestrial Fossil Record

Abstract

Insect and mite galls on land plants have a spotty but periodically rich and abundant fossil record of damage types (DTs), ichnotaxa, and informally described gall morphotypes. The earliest gall is on a liverwort of the Middle Devonian Period at 385 million years ago (Ma). A 70-million-year-long absence of documented gall activity ensues. Gall activity resumes during the Pennsylvanian Period (315 Ma) on vegetative and reproductive axial organs of horsetails, ferns, and probably conifers, followed by extensive diversification of small, early hemipteroid galler lineages on seed-plant foliage during the Permian Period. The end-Permian (P-Tr) evolutionary and ecological crisis extinguished most gall lineages; survivors diversified whose herbivore component communities surpassed pre-P-Tr levels within 10 million years in the mid-to late Triassic (242 Ma). During the late Triassic and Jurassic Period, new groups of galling insects colonized Ginkgoales, Bennettitales, Pinales, Gnetales, and other gymnosperms, but data are sparse. Diversifying mid-Cretaceous (125–90 Ma) angiosperms hosted a major expansion of 24 gall DTs organized as herbivore component communities, each in overlapping Venn-diagram fashion on early lineages of Austrobaileyales, Laurales, Chloranthales, and Eurosidae for the Dakota Fm (103 Ma). Gall diversification continued into the Ora Fm (92 Ma) of Israel with another 25 gall morphotypes, but as ichnospecies on a different spectrum of plant hosts alongside the earliest occurrence of parasitoid attack. The End-Cretaceous (K-Pg) extinction event (66 Ma) almost extinguished host–specialist DTs; surviving gall lineages expanded to a pre-K-Pg level 10 million years later at the Paleocene-Eocene Thermal Maximum (PETM) (56 Ma), at which time a dramatic increase of land surface temperatures and multiplying of atmospheric pCO2 levels induced a significant level of increased herbivory, although gall diversity increased only after the PETM excursion and during the Early Eocene Climatic Optimum (EECO). After the EECO, modern (or structurally convergent) gall morphotypes originate in the mid-Paleogene (49–40 Ma), evidenced by the Republic, Messel, and Eckfeld floras on hosts different from their modern analogs. During subsequent global aridification, the early Neogene (20 Ma) Most flora of the Czech Republic records several modern associations with gallers and plant hosts congeneric with their modern analogs. Except for 21 gall DTs in New Zealand flora, the gall record decreases in richness, although an early Pleistocene (3 Ma) study in France documents the same plant surviving as an endemic northern Iran but with decreasing associational, including gall, host specificity.

Insect herbivory immediately before the eclipse of the gymnosperms: The Dawangzhangzi plant assemblage of Northeastern China

“…Galling is a three‐dimensional growth on the surface of a plant organ that consists typically of an outer sclerenchymatous wall, and an inner zone of proliferating nutritive tissue that feeds the insect or mite inhabiting a central chamber. The gall is supplied by vascular tissue attached to the parent plant that is developmentally controlled by the galler (Labandeira, 2021). At DW, the 14 gall DTs are divided into five groups based mainly on shape, size, structure, position on the plant organ, and host tissue response.…”

“…3K), and on Agathis zamunerae Wilf (Araucariaceae) (Wilf et al ., 2014) from the early Eocene Laguna del Hunco Fm in Patagonia, Argentina (Donovan et al ., 2020 and its fig. 2K; Labandeira, 2021). DT116 on Czekanowskia sp.…”

“…Two deposits from the KTR have supplied plant assemblages that provide almost all of the plant–insect associational data for this time interval: the older late Barremian–early Aptian (126–122 Ma) Yixian Formation (Fm) from Northeastern China (Chang et al ., 2017), and the younger late Aptian (115–113 Ma) Crato Fm of Northeastern Brazil (Martill et al ., 2007). Previous studies of the Yixian Fm involved principally Liaoningocladus boii Sun, Zheng et Mei, a broadleaved, pinalean conifer for which herbivory has been documented occasionally as external foliage feeding (Ding et al ., 2015), oviposition (Ding et al ., 2015; Lin et al ., 2019), piercing and sucking (Ding et al ., 2015), mining (Ding et al ., 2014), and galling (Wong et al ., 2015; Labandeira, 2021). Co‐occurring broadleaved conifers Lindleycladus lanceolatus (L. et H.) Harris, and Podozamites sp.…”

Fossil Leaves of Meliosma (Sabiaceae) With Associated Pollen and a Eupodid Mite From the Eocene of Maoming Basin, South China

“…Analysis of plant interactions with arthropods and plant pathogens (especially fungi) in the fossil record provides recent ecological and evolutionary studies with comparative long-term data on the influence of climate change on the ecosystem structure and food-chain relationships (Currano et al, 2008;Wilf, 2008;Wappler, 2010;Wappler et al, 2012;Wappler and Grímsson, 2016), recovery of ecosystems after environmental crises and mass extinctions (Labandeira et al, 2002;Wilf et al, 2006;Wilf, 2008;Donovan et al, 2014Donovan et al, , 2016, and their evolutionary implications (Labandeira, 2013(Labandeira, , 2021Labandeira and Currano, 2013).…”

Community structure and specialization in fig wasps (Hymenoptera: Chalcidoidea) in a region of Cerrado

“…Specialization is ubiquitous in living systems, as species may occupy only a subset of habitats or hosts available (Forister et al, 2012). Ecological specialization may be described as a species' variance in performance across a given range of resources or impact across ranges of environments (Devictor et al, 2010), and such frameworks are pervasive in interactions established among plants, herbivorous insects, and their enemies through geological time (Labandeira, 2021;Labandeira and Li, 2021). Such interactions are classic models for studies of host specialization in insects (Forister et al, 2012).…”