CY501-C14[607-645].qxd 2/16/05 1:16 AM Page 607 quark11 27B:CY501:Chapters:Chapter-14: 14InsectsInsects Become Become Modern: The MCretaceousodern: and The Tertiary Periods is ambiguous and controversial, as we will soon discuss. THE CRETACEOUS CretaceousWithout question, and though, the angiosperm radiations opened The Cretaceous Period, 145–65 MYA, is one of the most signif- vast niches that insects exploited supremely well. icant geological periods for insect evolution of the seven The earth was geologically more restless during the Creta- major periods in which insects are preserved. Hexapods ceous than most times in its history. There was dramatic cli- appeared inTe the Devonian;r wingedtiary insects, in the Carbonif- Periodsmate change and tectonic activity, the latter of which resulted erous; and the earliest members of most modern orders, in in widespread volcanism and the splitting and drifting of the Permian to Triassic. In the Cretaceous, however, there continents. The fragmentation of Gondwana into the present evolved a nascent modern biota, amidst unprecedented southern continents 120–100 MYA is often invoked to explain geological and evolutionary episodes. Because the Creta- contemporary distributions of various plants and animals ceous is so much younger than the Paleozoic and earlier (including insects) that have closely related species occupy- Mesozoic periods, the fossil record of this period has been ing Australia, New Zealand, southern South America, and erased less by faulting, erosion, and other earth processes. southern Africa. Ancestors of these austral relicts purportedly Thus, Cretaceous fossils have left a particularly vivid record drifted with the continents, though some Cretaceous and of radiations and extinctions. Tertiary insect fossils indicate that many presently austral During the Cretaceous many modern families of insects groups were very widespread. The massive meteoritic impact first appeared, some of which appeared as early as the that ended the Cretaceous is well known for the extermina- Jurassic or even the Triassic. Others, like the families of tion of non-avian dinosaurs, ammonites, and other groups, schizophoran flies and ditrysian lepidopterans, are much but insects appear to have been little affected by this biotic younger, having evolved almost entirely in the Tertiary. It is Armageddon, at least at a gross level. As a result, the Creta- plausible that half or more of the Recent insect families ceous can uniquely inform us about how insects radiated, appeared in the Cretaceous, and this appears to be related as how they endured mass extinctions, and thus why they are both cause and effect to another biotic revolution of the time: such remarkably successful organisms. the radiation of angiosperms. There is no question that the approximately 250,000 FLOWERING OF THE WORLD: THE species of flowering plants comprise the dominant life form ANGIOSPERM RADIATIONS on land, though their origins approximately 130–140 MYA were very modest compared to their radiations some 20–30 Angiosperms appear to be closely related to a particular MY later. Without angiosperms, terrestrial existence would be group of “gymnosperms,” specifically the living, relict group far less colorful and entirely unrecognizable, which is why we Gnetales. Gnetaleans have a fossil record that extends more define almost all biomes on the basis of angiosperms, from than 60 MY before the earliest known angiosperms. Bennetti- heathlands and savannas to tropical rain forests. Insects were taleans (including the genus Pentoxylon) is an extinct group, the original partners of angiosperms, as pollinators and their which has also been proposed as the closest relatives of primary “predators” (i.e., herbivores), and insects remain the angiosperms. These plants resembled cycads and lived from most intimate and pervasive associates of angiosperms. It is the Triassic to the latest Cretaceous, and they had pollen- generally understood that pollinating insects facilitate and producing organs fused into a synagium; most were dioecious even control gene flow in most flowering plants, and thus (where the different sexual organs are on separate plants); must affect speciation of the plants, but how host plant spe- and they appear to have been insect pollinated (their repro- cialization could affect the speciation and diversity of insects ductive structures were even called “flowers”). Bennettitales 607 CY501-C14[607-645].qxd 2/16/05 1:16 AM Page 608 quark11 27B:CY501:Chapters:Chapter-14: 608 EVOLUTION OF THE INSECTS 14.1. One of the most profound biological episodes in the history of life was the radiation of flowering plants in the Cretaceous. Insects are the primary pollinators and consumers of angiosperms, and they have affected the evolution of each other more than have any other organisms. Here a small pyralid moth visits a coneflower (Rudbeckia) in Vermont. appear to be most closely related to cycads (W. L. Crepet, pers. comm.). Gnetaleans may be the living sister group to the angiosperms, or they may be closely related to conifers. Molecular evidence for a close relationship between gne- taleans and conifers is compelling (Hansen et al., 1999; Samigullin et al., 1999; Bowe et al., 2000; Chaw et al., 2000), yet other studies support their close relationship with angio- sperms (Doyle and Sanderson, 1997; Savolainen et al., 2000). These plants actually possess several morphological features distinctive to angiosperms that seem unlikely to have evolved convergently (Loconte and Stevenson, 1990; Nixon et al., 1994). There are three disparate genera of living gne- taleans. These include the cosmopolitan genus Ephedra with approximately 35 species (Figure 14.2), which superficially resembles horsetails (Equisetum), and the huge recumbant Welwitschia mirabilis. Both of these genera live in xeric regions, and Welwitschia in fact is restricted to the very dry Namib Desert in Africa. The other genus is Gnetum (Figure 14.3), the approximately 30 species of which are trees and vines found in the world’s tropics. Fossil gnetalean pollen occurs through much of the Mesozoic, but definitive macro- fossils of the group are known from the Early Cretaceous and 14.2. Reproductive structures of Ephedra antisyphilitica, a living member of the relict group Gnetales, which appear to be the closest later. living relatives of angiosperms, or possibly of the conifers according to Fortunately, our current understanding of the early evolu- recent molecular evidence. The small, sticky pollination droplets of gnetaleans not only capture wafting pollen but also attract insects and tion of angiosperms has been revolutionized in the past few may have led to the symbiosis between pollinating insects and flowers. decades by essentially three modes of inquiry. CY501-C14[607-645].qxd 2/16/05 1:16 AM Page 609 quark11 27B:CY501:Chapters:Chapter-14: INSECTS BECOME MODERN: THE CRETACEOUS AND TERTIARY PERIODS 609 earliest “roots” in the phylogeny of living angiosperms (Matthews and Donoghue, 1999; Qiu et al., 1999, 2000; Barkman et al., 2000; Zanis et al., 2002). The earliest fossil evidence of angiosperms is pollen 130–140 MYo preserved in Israel, Morocco, Libya, and possi- bly China, and the earliest macrofossils are slightly younger leaves and flowers some 120–130 MYO. The earliest remains are sparse but become progressively more abundant and diverse into the Cretaceous, which has led to the widespread belief that angiosperms originated in the earliest Cretaceous, 130–145 MYA. This leaves a huge gap between the earliest angiosperms and earliest gnetaleans and bennettitaleans, which some recent investigators have interpreted as a fossil record deficient for angiosperms. Estimates of angiosperm origins based on molecular divergence are typically far older than those estimates based on fossils, and range from the Jurassic, 180–160 MYA (Wikström et al., 2001), to even the Tri- assic (Li et al., 1989; Kenrick, 1999). Besides the usual prob- 14.3. Branch with microsporangia of the living gnetalean plant, Gne- tum gnemon. 1. The use of phylogenetics in studying the relationships of living and fossil angiosperms (Crane, 1985; Donoghue and Doyle, 1989; Doyle and Donoghue, 1992; Nixon et al., 1994; Bremer, 2000; Doyle and Endress, 2000). 2. Continuous discovery of Cretaceous fossils, but particu- larly the remarkably preserved and diverse fusainized flowers and fruits from Europe and North America (e.g., Friis et al., 1986, 1994, 1999; Drinnan et al., 1990; Nixon and Crepet, 1993; Crane et al., 1995; Crane and Heren- deen, 1996; Crepet and Nixon, 1998; Gandolfo et al., 1998) (e.g., Figure 14.4). Fusainized plant remains were pro- duced by fires, similar to the process of charcoalification, and they are preserved with microscopic fidelity. Prior to the discovery of intact, fusainized reproductive struc- tures the fossil record of angiosperms was largely rele- gated to pollen, leaves, and the occasional compressed flower. There are also a few beautifully preserved flowers in Cretaceous amber (Figures 14.5, 14.6). Important new deposits of Cretaceous compression fossils include those from the Yixian Formation of China (e.g., Sun et al., 2002) 14.4. Cretaceous flower exquisitely preserved as a carbonized replica and the Santana Formation of Brazil (Mohr and Friis, in 90 MYO clays from New Jersey. Remains of plants and animals 2000) (Figure 14.7). smothered under leaf litter were apparently rendered to charcoal by 3. The application of DNA sequences to large numbers of ancient forest fires, or fusainized. The discovery of diverse fusainized flowers from the Cretaceous has revolutionized understandings of the angiosperm taxa (APG, 1998; Savolainen et al., 2000; Soltis early evolution of angiosperms. Scanning electron micrograph. Photo: et al., 2000), and particularly to the identification of the W. L. Crepet. CY501-C14[607-645].qxd 2/16/05 1:17 AM Page 610 quark11 27B:CY501:Chapters:Chapter-14: 610 EVOLUTION OF THE INSECTS 14.5. An inflorescence in 90 MYO amber from New Jersey. It is one of the earliest records of the Fagaceae, which includes the beeches and oaks. Flowers in Cretaceous amber are extremely rare, and even fewer are as detailed as this.