The adaptive significance of insect gall morphology

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Abstract

Insect galls are dramatic examples of extended phenotypes: although composed of host plant tissues, their development is largely controlled by insect genes. Adaptive explanations for gall traits should thus be expressed in terms of impacts on insect fitness, but the extent to which interspecific variation in gall structure is adaptive, and the possible selective pressures driving diversification in gall form remain controversial. In colonial aphids and thrips, gall structures probably diversified in response to selection for enhancement of the surface area available for feeding. In other taxa, such as gall wasps and gall midges, diversity is expressed predominantly in non-nutritive tissues, particularly those on the gall surface. All natural enemies attack the occupants of closed galls by penetrating gall tissue, and modifications that reduce enemy attack rates should thus be favoured. Recent studies of intraspecific variation in gall form strongly support a defensive role for several traits, but, to date, there is little empirical support for enemies as a cause of interspecific variation in gall form. Selection imposed by enemies nevertheless remains the most probable adaptive explanation for the evolution of diversity. We suggest that this hypothesis has yet to be tested explicitly, and discuss the requirements for an appropriate cross-species analysis.

Section snippets

Gall diversity

Galling has evolved repeatedly among and within insect orders 1, 2, 3, producing species-rich lineages with fossil records extending back at least 300 million years 4, 5, 6, 7, 8. The apparent success of gall induction as a life-history trait has fuelled a continuing debate about the adaptive significance of gall induction and, in particular, of gall morphology 9, 10. This debate is fuelled by observations that insect galls commonly include tissue types that are absent from ungalled host plants

Galls as the extended phenotypes of galler genes

The molecular basis of gall induction remains unknown in all insect galls (Box 1) and the causal roles of the insect and the plant can often be inferred only indirectly. This is significant because, until the mechanisms are known, we cannot rule out the possibility that variation in gall complexity and diversity among galler lineages might, in part, be due to differences in galling mechanisms rather than differences in selective pressures. Evidence nevertheless suggests that gallers are

Hypotheses for the adaptive significance of gall induction

Of the hypotheses that have been advanced for the adaptive significance of gall induction 9, 10, three are relevant to discussions of gall morphology: the Nutrition hypothesis; the Microenvironment hypothesis; and the Enemy hypothesis. Testing these hypotheses involves two challenges. The first is to explain the adaptive value of gall induction over other modes of insect herbivory (e.g. leaf-mining or exposed feeding), and so the evolution of the first galls. The second is to identify processes

The Nutrition hypothesis

The Nutrition hypothesis states that galls provide enhanced nutrition over other feeding modes. With the exception of fungus-feeding gall midges, gallers feed on plant tissues or fluids. Many galls contain highly differentiated nutritive tissues (Figure 3) that are both more nourishing and less well defended than are non-gall tissues on the same plant (Box 1) 1, 9, 10, 14, 22, 25, and enhanced nutrition is widely accepted as a general advantage of gall induction 9, 10. The Nutrition hypothesis

The Microenvironment hypothesis

The Microenvironment hypothesis states that gall tissues act to protect the galler from unfavourable abiotic conditions, particularly desiccation 3, 9, 10, 22, 25, 26, 27, 28. Gallers that occupy partially enclosed structures lie within the boundary layers of moist air surrounding plant structures, and those developing within plant tissues are often directly bathed in fluid and so are buffered against water stress 1, 25, 26. This hypothesis is widely accepted as a selective advantage of gall

The Enemy hypothesis

The Enemy hypothesis maintains that galls protect gallers from attack by natural enemies. In fully enclosed galls, all attacks must take place through gall tissues, and selection should then favour any modifications of gall morphology that enhance galler survival. Galls do provide some protection against attack by nonspecialist predators and pathogens [30], but they are far from being enemy-free space: most are attacked by communities of specialist enemies (including fungi, and the larvae of

Natural enemies and interspecific variation in gall morphology

As discussed, neither the Nutrient hypothesis nor the Microenvironment hypothesis can explain the diversity in external gall structures induced by members of a given group of gallers on the same part of the same host plant at the same time (Figure 4). However, there are reasons to believe that selection imposed by natural enemies could, in principle, explain both the evolution and the maintenance of such diversity [37] (Box 5). For this hypothesis to be accepted, two general predictions must be

Conclusions and goals of future research

Gall morphologies represent the extended phenotypes of galler genes, and adaptive explanations for them should be expressed in terms of galler fitness. All galls provide high-quality nutrition and protection from microclimatic fluctuation, but they do not represent enemy-free space. Diversification of some internal gall structures has probably been driven by enhancement of nutritive supply, whilst improved defence is the most probable adaptive explanation for diversification of external gall

Acknowledgements

We thank colleagues for helpful discussions, particularly György Csóka, Jose-Luis Nieves-Aldrey, Juli Pujade-Villar, George Melika, William Foster, Rachel Atkinson, Antonis Rokas, Richard Bailey, Alex Hayward, Lisa Harper, Jens-Peter Kopelke, Utako Kurosu, Tom Chapman, Dick Askew and James Cook. We thank James Cook, Bernie Crespi and an anonymous referee for constructive comments. Work on cynipid galls by G.N.S. and K.S. is supported by UK Research Council NERC grants GST/032035, GR3/12947 and

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