Evidence for an Earliest Late Carboniferous Divergence Time and the Early Larval Ecology and Diversification of Major Holometabola Lineages Author(S) :Conrad C
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Evidence for an Earliest Late Carboniferous Divergence Time and the Early Larval Ecology and Diversification of Major Holometabola Lineages Author(s) :Conrad C. Labandeira Source: Entomologica Americana, 117(1):9-21. 2011. Published By: The New York Entomological Society DOI: http://dx.doi.org/10.1664/10-RA-011.1 URL: http://www.bioone.org/doi/full/10.1664/10-RA-011.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Entomologica Americana 117(1/2):9–21, 2011 EVIDENCE FOR AN EARLIEST LATE CARBONIFEROUS DIVERGENCE TIME AND THE EARLY LARVAL ECOLOGY AND DIVERSIFICATION OF MAJOR HOLOMETABOLA LINEAGES 1,2,3 CONRAD C. LABANDEIRA 1Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA 2Department of Entomology and BEES Program, University of Maryland, College Park, MD 20742, USA Abstract.—Four fossil taxa of earliest Holometabola recently were identified based on a variety of determinative evidence and assigned to a stem-group or a basal lineage within a modern order. One consequence of these new discoveries is that the divergence date between the Holometabola and its sister clade has been set earlier than previously thought on the basis of fossils or molecular phylogenetic evidence. This new date provides a minimal calibration date pegged to the Early Carboniferous–Late Carboniferous boundary, and approximates an absolute date of 318 million years. The four taxa provide new insights into the life habits, particularly feeding habits, of early holometabolan larvae. Additionally, they require an explanation of why there is an 80 million year lag between the origin and the taxonomic dominance of this profound developmental innovation in early terrestrial ecosystems. An earlier lead time is likely present for these earliest holometabolan fossils, which can be extrapolated conservatively to the Late Mississippian, 328 to 318 million years ago. Consequently, a focused investigation on earlier, Late Mississippian strata to search for ancestral holometabolan insects is imperative. INTRODUCTION condition, from both an intrinsic, evolutionary developmental perspective that accounts for the Perhaps the most significant issue in the study origin of the larval and pupal stages, and from the of fossil insects has been the origin of the regional or global environmental conditions Holometabola. The Holometabola, also known during the late Paleozoic that would have selected as the Endopterygota, are characterized by for holometabolous traits (Lameere, 1908; Hin- complete metamorphosis in which a larva hatches from an egg, undergoes several discrete growth ton, 1963; Sehnal et al., 1996; Truman and increments, eventually becomes a pupa, typically Riddiford, 1999; Nel et al., 2007). These three the resting stage, and ends as an emergent adult. features circumscribe the principle issues defining Considerable attention has been devoted toward the early history of the Holometabola, and until understanding three features of the currently recently, there has been minimal progress on all highly speciose Holometabola. First has been the three fronts. However, recent concerted efforts timing of the origin of the Holometabola during have narrowed the compass of possibilities for the late Paleozoic (Hennig, 1969; Kukalova´-Peck, addressing these issues and, in some cases, have 1997; Gaunt and Miles, 2002; Nel et al., 2007; provided surprising results in determining when Wiegmann et al., 2009). Second, there have been the Holometabola initially diversified, the groups many attempts to identify taxa that comprised the or clades that constituted the earliest Holometa- earliest holometabolans, either from morpholog- bola, and the selective advantage of the endopter- ical or evolutionary developmental traits of the ygote condition over other insect developmental modern taxa or from phylogenetic inference based patterns under late Paleozoic and Triassic envi- on fossil occurrences (Hornschemeyer, 2002; ronmental conditions. Whiting, 2004; Nel et al., 2007; Be´thoux, 2008; The distinctive developmental trajectory that Wiegmann et al., 2009). Third, considerable effort defines the Holometabola is contrasted with the has been devoted toward understanding the hemimetabolous condition. Under hemimetabo- processes that resulted in the endopterygote lous development, an egg directly hatches into a series of discrete nymphal stages that largely resemble and give rise to the adult stage, which 3 Email address for correspondence: [email protected] also can be compared to the ametabolous 10 ENTOMOLOGICA AMERICANA Vol. 117(1/2) condition characterized by minimal developmen- more widely supported and accounts for larval tal change. Insects with holometabolous develop- structures such as abdominal prologs as subse- ment currently are the most diverse clade of quently derived structures (Sehnal et al., 1996), the multicellular organisms, consisting of approxi- nymphal replacement hypothesis better explains mately 766,100 described living species (Davis et origin of complete metamorphosis as a modifica- al., 2010), although the total number is probably a tion of embryonic stages (Truman and Riddiford, several-fold multiple of that figure (Kristensen, 1999). The consequence of these profound, 1999). The Holometabola presently constitute developmental changes was that holometaboly about 82.7 percent of all insects, and probably immediately provided larval-feeding and adult- have been the dominant clade of insects since the reproductive adult instars access to very different mid Triassic. When considered as a group, the habitats that often were deployed in a seasonal or Holometabola has invaded every terrestrial and other spatiotemporally exclusive manner—thus freshwater habitat and have made considerable allowing survival of both during mutually unfa- inroads along marginal marine–land and marine– vorable conditions. air interfaces (Wheeler, 1990; Mayhew, 2007). The principal goal of this contribution is to Collectively, they have an amazingly broad provide divergence times from recent evidence dietary repertoire, and include taxa that range that document the presence of holometabolous from detritivores and other decomposers, micro- taxa during the Late Carboniferous Period, herein vores, fungivores to especially herbivores, but also equivalent to the Pennsylvanian Subperiod (Ogg are consumers of animals as predators, parasit- et al., 2008). Four recent reports indicate that oids and parasites and inhabit unusual habitats structurally varied larval and adult Holometa- such as oil seeps, playa lake brines, and hot bola, representing four distinctive taxa, were springs (Wheeler, 1990; Kristensen, 1999; Laban- present during Pennsylvanian times. A related deira, 1999, 2002). objective is to place these taxa in a relevant One of the key features of the holometabolous temporal context and to indicate the early larval condition is the developmental and ecological ecology of the Holometabola. Last, a discussion separation of their life cycle into a feeding stage, ensues regarding the selection pressures affecting the larva, which typically bear working mouth- these earliest known taxa during an interval of parts for the bulk processing food but lack major environmental change. capabilities for mating and flight, versus the reproductive stage, the adult, which is endowed METHODS with locomotory organs of functional wings and Several reports have mentioned Pennsylvanian legs, and genitalia that efficiently complete repro- age Holometabola. Four taxa from these reports duction. The distinctive larva undoubtedly origi- are accepted (Fig. 1) and are positioned on a nated from a hemimetabolous mode of develop- recent, well-supported cladogram (Wiegmann et ment once in the history of insects, albeit in one of al., 2009) as proximal as possible to their inferred two ways (Truman and Riddiford, 1999). The insect order or stem-group (Fig. 2), based on nymphal replacement hypothesis (Berlese, 1913; characters and taxonomic assignments from the Imms, 1937) proposes that the new larval instar respective descriptions. Accordingly, the earliest emerging from the insect egg essentially became a occurrences of many holometabolous clades had feeding embryo and progressively overtook the to be moved downward, earlier in time, to feeding responsibilities of successive nymphal accommodate not only long-known Early Perm- instars, such that nymphal instars were reduced ian fossils, but also the four earlier holometabo- to a single instar that became the pupa in lous occurrences mentioned herein (also see Davis holometabolous development. Alternatively, the et al.,