Foraging  Behaviour  and  the  Evolution  of  Specialisation  in  Herbivorous  Arthropods

In Part One of this thesis, I extend the theory on evolution of specialisation. Chapter 2 provides an evolutionary analysis of a model by Wilson and Yoshimura (1994), which predicts the stable coexistence of two specialist and one generalist species in two habitats that vary temporally in their carrying capacity. The objective is to assess whether such coexistence may arise through gradual evolutionary change. Chapter 3 changes the stage from a discrete set of habitats to a continuous distribution of resources in a gradient of plant quality. The combined evolution of specialisation and feeding range in the gradient generically produces an adaptive radiation (see Schluter 2000) of herbivore species over the resource gradient in this model. With respect to the level of foraging specificity required, a common conclusion from the two Chapters is that almost any level will do (depending on the strength of the fitness trade-off). Foraging behaviour does not place a strong constraint on the evolution of specialisation.

In Part Two, I investigate the foraging behaviour of the two-spotted spider mite Tetranychus urticae. In particular I test the assumption on flexible foraging behaviour in the models of Part One: depending on the available resources and the number of competitors on each resource, consumers decide where they forage. This implies that they learn which resources are available in the environment, and that they assess their performance on a resource. Several experimental studies in this thesis show that T. urticae is able to learn: it changes behaviour with experience. Moreover, the results are consistent with the idea that foraging decisions of T. urticae individuals are based on performance on its resource.
In Chapter 4, I show that T. urticae learns to prefer cucumber over tomato in a multiple-choice test and that this improves fitness of the individual mites, because cucumber allows for a higher oviposition rate and an increased survival rate of adult females, as well as increased survival and developmental rate of their offspring. In Chapter 5, I show that spider mites can even distinguish plant quality: they learn to prefer cucumber plants with a lower degree of feeding damage, which sustain a higher oviposition rate of adult females and higher offspring survival.
Chapter 6 provides evidence of induced preference, as well as induced performance on tomato plants in various strains of T. urticae. The spider mites probably achieved induced performance by switching on detoxification mechanisms which allowed them to cope with the toxins incurred from feeding on tomato plants. The induced performance may subsequently be the cue that leads to increased (i.e., induced) preference for that host plant.
In Chapter 7, I present experiments aimed to unravel the spatial scale at which learning about the host plant changes the foraging decisions and thereby the distribution of mites over different host plants. The results of these experiments show that leaf-to-leaf contact was required for spider mites to switch from thebad host plant (tomato) to the good one (cucumber) - at this small scale, though, switching readily occurred. Without contact between plants, the travel costs seem to be too high for the benefit of exploiting a higher quality food plant.

In Part Three of this thesis, I shift the emphasis to mechanisms that may promote speciation through specialisation. Chapter 8 focuses on Wolbachia, a group of obligately endosymbiotic bacteria widespread in insects, but also infecting other arthropods like mites and crustaceans (Stouthamer et al. 1999). One of the main effects of Wolbachia infection is cytoplasmic incompatibility (CI): infected males are reproductively incompatible with uninfected females. Interestingly, CI is Wolbachia-strain specific. Consequently, two different Wolbachia strains can be mutually incompatible (bidirectionally incompatible; biCI). Therefore, if two populations of a species are locally specialising and become infected with two such biCI Wolbachia strains, they may be instantaneously reproductively isolated. Recent reports show that Wolbachia can have an important role in reproductive isolation in nature (Shoemaker et al. 1999; Bordenstein et al. 2001). However, we still do not have a good understanding of how one strain of Wolbachia is able to spread through populations of its host - a necessary basis for investigation into the conditions under which Wolbachia-induced bidirectional incompatibility may play a role in speciation of its host.
In Chapter 8, I investigate the conditions that lead to infection of a host species with CI-Wolbachia, assuming that infection bears a fitness cost. Traditional, single-species models predict that there is a threshold frequency for invasion: if the infection exceeds this threshold it can spread, but below it the infection goes extinct. However, an infection in a population will usually start with one infected female - well below the invasion threshold. Still, many populations sampled in nature are infected. Usually, it is assumed that drift carries the Wolbachia infection over the threshold, but in Chapter 8 we show that drift does not increase the probability of infection to levels high enough to account for the frequencies of infected populations observed. Alternatively, we offer three additions to the theory that may allow Wolbachia infections to spread even when rare: metapopulation structure, sex ratio effects, and other fitness-compensating effects.
Chapter 9 contains the synthesis of this book, where I review several conditions promoting adaptive speciation (through specialisation) in agricultural pests. Adaptive speciation, as explained above, is used to describe the process where evolution promotes the splitting up of one species in two (evolutionary branching) through disruptive selection arising from the ecological feedback on the growth rate of individual phenotypes. The chapter provides an argument why agricultural pests are excellent objects for studying adaptive speciation, as exemplified by research on model systems such as the apple maggot fly Rhagoletis pomonella (Feder 1998), the pea aphid Acyrthosiphon pisum (Via 2001) and the two-spotted spider mite Tetranychus urticae (Gotoh et al. 1993) (but also the fall armyworm Spodoptera frugiperda [Pashley Prowell 1998]). The topics discussed include adaptive learning and its effects on foraging behaviour, adaptive mate choice and CI-Wolbachia. Premating barriers due to adaptive learning of host plant quality and adaptive mate choice and post-mating barriers due to symbiont-induced incompatibilities may well play a major role in the emergence of novel host races among arthropod pests in agriculture.


References

• Bordenstein, S., F.P. O'Hara, and J.H. Werren (2001). Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409: 707-710.
• Feder, J.L. (1998). The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In: Endless Forms: Species and Speciation (eds. D.J. Howard, S.H. Berlocher) Oxford: Oxford University Press; pp 130-144.
• Gotoh, T., J. Bruin, M.W. Sabelis, and S.B.J. Menken (1993). Host race formation in Tetranychus urticae: genetic differentiation, host plant preference and mate choice in a tomato and a cucumber strain. Entomologia Experimentalis et Applicata 68: 171-178.
• Pashley Prowell, D. (1998). Sex linkage and speciation in Lepidoptera. In: Endless Forms: Species and Speciation (eds. D.J. Howard, S.H. Berlocher) Oxford: Oxford University Press; pp 309-319. Schluter, D. (2000). The Ecology of Adaptive Radiation. Oxford: Oxford University Press.
• Shoemaker, D.D., V. Katju, and J. Jaenike (1999). Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53: 1157-1164.
• Stouthamer, R., J.A.J. Breeuwer, and G.D.D. Hurst (1999). Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53:71-102.
• Via, S. (2001). Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology & Evolution 16: 381-390.
• Wilson, D.S., and J. Yoshimura (1994). On the coexistence of specialists and generalists. American Naturalist 144: 692-707.

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