Plant hybrid zones and insect host range expansion - Hybridization and Resistance to Parasites

Ecology, March, 1999 by Diana Pilson

INTRODUCTION

Most herbivorous insects are specialized to some degree (Price 1980, Fox and Morrow 1981, Strong et al. 1984). Some species feed on hosts in just a few families or genera, while others are extreme specialists and feed on only one to a few species. It is these extreme specialists that have most fascinated insect ecologists. With so much potential food available why do they limit feeding to such a narrow subset of potential hosts? One suggestion is that specialization is an evolutionary dead end: generalists and specialists might be equally likely to evolve, but, once specialized, insects might have difficulty "escaping" to a more generalized state (Rausher 1993). As a mechanism to allow specialized insects to expand their host range Floate and Whitham (1993) proposed the hybrid bridge hypothesis, which suggests that hybrid intermediates facilitate expansion of the host range to include previously unused species. The objective of this essay is to evaluate the hybrid bridge hypothesis in light of existing theoretical and empirical work on the evolution of insect host range.

THE HYBRID BRIDGE HYPOTHESIS

Floate and Whitham (1993) hypothesize that plant hybrids "bridge" the genetic gap between actual and potential host species, and therefore make it more likely that the insect will evolve an expanded host range. Thus an [F.sub.1] plant, which has an intermediate genotype, is assumed to also have an intermediate phenotype for characters (e.g., morphology or chemistry) that affect insect host use. Further, they suggest that backcross plants (BC), which contain more of the original host's genome than [F.sub.1] plants, provide a bridge between pure hosts and [F.sub.1]s. Additionally, more complex BC plants provide smaller "bridges" for insects to cross. Thus, Floate and Whitham (1993) hypothesize that insects can adapt in small steps to the alternate host's genome. Following this logic, they suggest that the more continuous the distribution of hybrid genotypes, the more likely it is that an insect will expand its range to include the alternate host. As evidence in support of their hypothesis, they document densities of seven gall-forming aphids and one gall-forming mite on two species of Populus, putative [F.sub.1] plants, and complex backcrosses to one of the parents. They find that aphid and mite species with a normal host that backcrosses with the hybrids are found on the hybrids, as well as on their own host. However, the aphid species with a normal host that does not backcross with the [F.sub.1]s feed only on their normal host. Floate and Whitham (1993) suggest that this is because the genetic gap between the host and the [F.sub.1] is large relative to the two smaller genetic gaps: (1) between the parent and the BC, and (2) between the BC and the [F.sub.1].

However, their model contains two critical, but unstated, assumptions. The first is that phenotypic gaps between actual and potential hosts limit host range in herbivorous insects and mites, and the second is that the genetic control of characters controlling host use is additive in all types of hybrids. In addition, the hypothesis ignores the distinction between insect preference for a host plant and physiological performance once on a host. Because the hybrid bridge hypothesis provides a new mechanism to allow host range expansion, the hypothesis, as well as these assumptions, is best evaluated in the context of theoretical and empirical work on the evolution of host range in herbivorous insects. Although still relatively poorly understood, some conditions favoring host shifts, host range expansion, and specialization have been elucidated. Host range expansion onto hybrids, like range expansion onto novel hosts, must be controlled by relative differences in preference and performance on the ancestral and novel hosts. Thus, these hypotheses would benefit from integration.

EVOLUTION OF SPECIALIZATION

An important cost of host specialization is decreased food availability. Thus, to the extent that feeding larvae or adults run out of food, or ovipositing females are unable to locate host plants on which to place their eggs, there will be selection for increased host range (Futuyma 1991). Moreover, because some individuals probably run out of food in every generation, there is likely to be continuous selection to increase host range. In the face of such selection, what factors maintain the relatively narrow host specificity of most herbivorous insects?

One explanation is that negative pleiotropic effects of loci controlling digestive efficiency or detoxification mechanisms prevent simultaneous adaptation to multiple hosts. However, this "jack of all trades is a master of none" explanation has found only modest support (reviewed by Jaenike 1990, Futuyma and Keese 1992). While some studies have found negative correlations between herbivore performance on two hosts (Gould 1979, Fry 1990, Karowe 1990, Via 1991, Mackenzie 1996), others seeking such trade-offs have not been successful (Rausher 1984b, Via 1984, Hare and Kennedy 1986, Futuyma and Phillipi 1987, James et al. 1988, Jaenike 1989, Fox 1993). For example, Futuyma and Phillipi (1987) found mostly positive correlations between larval survival and weight of Alsophila pometaria reared on four tree species. Although in all of these studies performance is typically better on some hosts than others, positive correlations between performance measures suggest that there is no genetic constraint to simultaneous adaptation to multiple hosts. Joshi and Thompson (1995) note that many of the studies purporting to find no trade-offs between performance on different hosts were conducted either in a novel environment or on a normal and a novel host. In these situations alleles for general vigor are expected and are likely to obscure any underlying trade-off. Of course, as Joshi and Thompson (1995) also note, when an insect moves into a new habitat or onto a novel host, such general-vigor alleles may have important effects on the initial evolution of expanded host range. In sum, these studies suggest that host range must frequently be limited to only a few species by some factor other than physiological trade-offs.