Patterns of Development in Insect Parasites

M. Mackauer Centre for Pest Management Department of Biological Sciences Simon Fraser University Burnaby, British Columbia, Canada

R. Sequeira1 Centre for Pest Management Department of Biological Sciences Simon Fraser University Burnaby, British Columbia, Canada

I Introduction

Successful parasitism by insect parasitoids2 requires the solution of three kinds of general problems: (1) which host to select; (2) how to integrate development and growth with those of the host; and (3) what life-history tactics to adopt. The first problem concerns behavioral adaptations relating to host selection and progeny allocation by the adult female (Charnov and Skinner, 1985; Waage and Godfray, 1985; van Alphen and Vet, 1986; Waage, 1986) and will not be considered here for this reason. Instead we will focus mainly on the third and, to a lesser extent, the second problem, both of which concern parasite growth and development.

Most early studies have emphasized mechanisms of parasite growth and development, with less attention paid to the adaptive significance of these mechanisms. In a causal approach, parasite development and growth may be characterized in terms either of the effects of parasitism on the host (e.g., Doutt, 1963; Salt, 1964; Smilowitz and Iwantsch, 1973; Cloutier and Mackauer, 1979, 1980; Lawrence, 1982; Thompson, 1982, 1983; Beckage and Templeton, 1985, 1986; Strand, 1986; Gunasena et al., 1989; Vinson, 1990; Strand and Dover, 1991) or of the parasite’s response to variations in the nutritional state and physiology of the host (e.g., Corbet, 1968; Weseloh, 1984; Hébert and Cloutier, 1990; Lawrence, 1990; Kouamé and Mackauer, 1991; Strand etal., 1991; Sequeira and Mackauer, 1992a,b). In this regard, Lawrence (1986, 1990) considered host regulation (Vinson, 1975; Vinson and Iwantsch, 1980a) and flexibility of parasite development (Corbet, 1968; Weseloh, 1984) as alternate developmental strategies. This viewpoint stresses proximate mechanisms of parasite survival based on qualitative descriptions of the physiological and biochemical interactions between the parasites and their hosts.

However, functional constraints on the parasite’s growth and development on or in different hosts can also be considered as variables within a broader evolutionary framework. This approach emphasizes questions about the fitness value of developmental characteristics and patterns of host utilization. Because protelean parasites depend exclusively on host-derived nutrients for their larval development and growth, natural selection would be expected to favor mechanisms that maximize the efficient utilization of these resources. Optimal resource allocation to adult body size, considered the perhaps most important component of Darwinian fitness in parasitic wasps (King, 1987), depends on the insect’s growth rate and development time. The allocation of limited (host) resources to competing fitness functions may result in trade-offs that determine an “optimal character set” and, in doing so, may shape the evolution of a species’ life-history strategy (Sibly and Calow, 1986).

We use the term strategy in accordance with Dominey (1984) to refer to a set of general rules that specify which alternative pattern of responses will be adopted in a particular situation; these rules are typical for each species and determine its adaptedness to the environment, here the host. Tactics, by contrast, refer to several alternative options or mechanisms by which these evolutionary objectives are achieved; these option sets may vary among different individuals or phenotypes. Also, we distinguish between host suitability (Salt, 1938; Vinson and Iwantsch, 1980b) and host quality, two terms often used synonymously. A host species is suitable if it normally supports the successful development of parasite offspring; consequently, suitability is a characteristic of the host species and is genetically determined, or largely so. In comparison, we use the term quality to describe variations in the state or condition of the host that affect process dynamics, such as the rates of parasite growth and development. Such state variables include, or may be correlated with, host age, stage of development, size, sex, and nutritional status.

The chapter is organized as follows. First, we introduce the idiobiont–koinobiont dichotomy, which we use as a (macroevolutionary) organizing scheme. Second, we describe several developmental patterns that characterize broad differences between idiobiont and koinobiont parasites. Next, we discuss seasonal adaptations and the influence of host nutrition on parasite development, including superparasitism and starvation. Finally, we propose three models of parasite development in response to host constraints. We suggest that the essential components of any developmental strategy are the parasite’s growth rate, development time, and adult biomass, which are constrained by host quality in an association-specific manner.

II The Idiobiont–Koinobiont Dichotomy

Haeselbarth (1979) first drew attention to an important macroevolutionary division between parasites developing in hosts that continue to grow and metamorphose during the initial stages of parasitism (called koinophytes) and those that develop in nongrowing and paralyzed hosts (called idiophytes). Askew and Shaw (1986) introduced the terms koinobiont and idiobiont to describe these alternative host-exploitation strategies.

Because the host of an idiobiont does not feed, grow, or metamorphose during the course of the interaction, it contains a fixed amount of resources for the parasite larva, with large hosts being assumed of higher quality than small hosts. However, unless the host is killed by the female at oviposition, age-related variations in quality may result from developmental changes within a particular host stage, such as eggs and pupae (Strand, 1986; King, 1990a). By contrast, hosts parasitized by a koinobiont continue to feed, grow, and develop during much of the interaction. Consequently, host quality as a resource for the parasite larva is influenced by future host growth, which depends on the host’s age and stage of development, rather than on its size, at the time of parasitization (Mackauer, 1986; King, 1989; Kouamé and Mackauer, 1991; Sequeira and Mackauer, 1992a).

Blackburn (1991) noted that koinobionts have longer pupal periods and preadult life spans than idiobionts, suggesting that these two groups have probably evolved under different constraints with regard to resource usage. Askew and Shaw (1986) compared idiobiont and koinobiont strategies as a correlate of host range. They proposed that koinobionts are more likely to show a narrow specialization because of their greater dependence on host physiology and development. Gauld and Bolton (1988) noted that idiobionts typically are synovigenic (i.e., females mature eggs continuously throughout life), produce relatively large, lecithal (or anhydropic) eggs containing sufficient resources for early embryonic development, and develop as ectoparasites on concealed hosts. Koinobionts, by contrast, are typically endo-parasites, produce small nutrient-poor, alecithal (or hydropic) eggs, and attack free-moving hosts.

Idiobiont and koinobiont strategies show poor correlation with solitary and gregarious development (Askew and Shaw, 1986). Theoretical results (Godfray, 1987), and some experimental evidence (Cruz, 1981), suggest that solitary and gregarious development represent distinct reproductive and/or developmental strategies (Waage, 1986). However, many groups of parasites, including several genera such as Cotesia, contain both solitary and gregarious species. In most cases it is not clear whether such developmental variations are due to host-related conditions (le Masurier, 1987, 1991) or reflect phylogenetic constraints (Gauld, 1988; Gauld and Bolton, 1988), or both.

III Patterns of Parasite Development and Growth

A species’ life-history strategy represents a unique combination of responses (tactics) that are shaped by natural selection from an option set associated with each phenotypic character. Option sets may be empirically defined as the quantitative responses of their...