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The evolution of leaf mining: ecological constraints on adaptive radiation?

Session leader: Mike Singer.

Leaf mining is a feeding habit defined by consuming "live foliage while simultaneously dwelling inside it" (Connor and Taverner 1997). In practice, a leaf mine can be distinguished from most other forms of herbivory by the presence of at least partially intact epidermal layers on both surfaces of a leaf at the site of damage (Hering 1951). Leaf mines are usually visible on the exterior of the leaf as serpentine paths, blotches, or other characteristic shapes of discolored tissue. Mines may be occupied throughout an insect's feeding life, or may be abandoned for other feeding habits at some point in development. In the latter cases (exclusively lepidopterans), the earliest stages typically mine, giving way to different feeding habits in later stages (Hering 1951). Some leaf miners (especially larger leaf-mining lepidopterans) excavate more than one mine during the course of development. Most, however, develop completely inside a single mine. In comparison to external folivores, leaf miners are relatively small insects, physically constrained by the thickness and area of leaves they occupy.

Within the insects, there are approximately 10,000 described species of leaf miners. The habit is known from taxa in 51 families, but only in larvae of the holometabolous orders Coleoptera, Diptera, Hymenoptera, and Lepidoptera (see Table 3 in Connor and Taverner 1997). Lepidoptera includes more leaf mining families and species than any other order (Hespenheide 1991). Even without a resolved phylogenetic relationship among these orders, it is confidently assumed that leaf mining has independently evolved within each. In light of estimated phylogenies based on currently accepted classification, leaf mining has probably evolved more than 4 times in Coleoptera, at least 6 times in Diptera, and 6 times in Hymenoptera (Connor and Taverner 1997). However, it may have evolved only once in Lepidoptera (Labandeira et al. 1994, Powell et al. 1997). In all cases, leaf mining appears to be derived from other feeding habits, both external and internal forms of herbivory.

The convergence of leaf mining among distantly related lineages tempts one to examine its pattern of evolution from a phylogenetic point of view, and to consider ecological processes through which natural selection has constrained or spurred its radiation. By comparing the relative number of species in clades of the same age (sharing a common ancestor), Connor and Taverner (1997) found that leaf mining clades have fewer species than sister clades of external folivores. This pattern suggests constraints on the radiation of leaf mining relative to ectophagy.

Several ecological hypotheses have been advanced to explain the adaptive significance of leaf mining, most recently by Connor and Taverner (1997) (Table 1), but how ecological tradeoffs affect speciation is unclear. Numerous possibilities exist. For example, the extinction rate of leaf miners might be high relative to external folivores if ecological factors constrain population size, thereby increasing the probability of population extinction. Several ecological factors may impose mortality regulating population size (Table 2). Recent analyses of mortality for many taxa of leaf miner reveal that parasitoids and, in early life stages, plant factors are important (Cornell and Hawkins 1995, Hawkins et al. 1997). Alternatively, there may be constraints on leaf miner speciation rates relative to ectophages. Perhaps their intimate associations with host-plants reduce the probability of colonizing new hosts upon which they differentiate into new species. Or small size and short lifespan limits the dispersal ability of leaf miners and the likelihood of founding populations in geographically isolated areas.

Table 1. Hypotheses to explain the adaptiveness of leaf mining

Table 2. Sources of mortality that have possibly constrained leaf miner radiation

Another window into the history of leaf mining, the fossil record provides evidence that leaf mining occurred by the late Jurassic (ca. 150 mya) in the Lepidoptera, and possibly earlier if leaf mining represents the ancestral condition for the Heterobathmiina+Glossata clade (Labandeira et al. 1994). The frequency of fossilized leaf mines dramatically increases during the Cretaceous, coincident with the radiation of angiosperms (Labandeira et al. 1994). Lineages with leaf mining taxa in Coleoptera, Diptera, and Hymenoptera are also thought to have originated during the Cretaceous (Crowson 1981, Gauld and Bolton 1988), but little information is available for origins leaf mining clades themselves. Interestingly, clades of hymenopteran parasitoids of leaf miners (e.g. Eulophidae and other Chalcidoids) are inferred to have their earliest origin during the Cretaceous (Gauld and Bolton 1988), and probably radiated explosively during the late Cretaceous/early Tertiary periods.

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Copyright 1998, Michael Singer.