Divergent Host Relationships of Males and Females in the. Parasitoid Encarsia porteri (Hymenoptera: Aphelinidae). MARTHA S. HUNTER,1 MIKE ROSE, AND ...
ARTHROPOD BIOLOGY
Divergent Host Relationships of Males and Females in the Parasitoid Encarsia porteri (Hymenoptera: Aphelinidae) MARTHA S. HUNTER, 1 MIKE ROSE, AND ANDREW POLASZEK2 Department of Entomology, Texas A&M University, College Station, TX 77843
Ann. Entomol. Soc. Am. 89(5): 667-675 (1996) ABSTRACT "Heterotrophic" parasitoids have been reported in the aphelinid genus Encarsia. These are species in which females develop as primary internal parasitoids of whitefly and males develop as primary internal parasitoids of lepidopteran eggs. The obligate nature of the host relationships in these aphelinids has been questioned and was investigated in this study. We examined the oviposition of female Encarsia porteri (Mercet) in 3 host types: bollworm eggs (Helicoverpa zea (Boddie)), sweetpotato whitefly nymphs (Bemisia tabaci (Gennadius)), and early pupal wasps (E. porteri). Although males of most Encarsia species develop on wasp pupae as hyperparasitoids, female E. porteri did not generally oviposit in wasp pupae. Whitefly nymphs were parasitized almost exclusively by mated females, whereas both mated and unmated females oviposited in moth eggs. The suitability of the above hosts as well as pupal E. fonnosa were also investigated for the development of male progeny. Males were produced only on moth eggs. Thus, we conclude that the heterotrophic host relationships of E. porteri are indeed obligate. Larval E. porteri are sexually dimorphic. Early instars of male larvae have a sculptured cuticle, bear long spines along the venter, and have horn-like projections on the head capsule. Females, in contrast, are more typically hymenopteriform with weak sclerotization of the head capsule, indistinct segmentation, and a smooth cuticle. Also, although both male and female early instar larvae are enclosed within a membrane, only females are enveloped by an opaque cellular layer within this membrane. KEY WORDS Bemisia tabaci, heteronomous, heterotrophic, hyperparasitism, sexual dimorphism, host relationships
2 OR more disparate kinds of food or habitat are required to maintain a population, the resources are generally used in sequence by morphologically specialized life stages. Less commonly, male and female immature stages may be specialized on different resources; these systems have been called "heteronomous" by Walter (1983a). In heteronomous species, male and female larval morphology and behavior may be very different and may evolve more or less independently (Slatkin 1984). Like systems in which morphological specialization occurs within the same sex but in different generations, the evolution of sexual dimorphism in heteronomous species is not subject to the same sorts of developmental constraints as in species with sequential specialization. Multigenerational and heteronomous morphological specialization is constrained only by the different forms having genes in common (Moran 1994). Among multicellular animals, the heteronomous biology appears to be confined to 2 parasitic insect lineages; one family of Strepsiptera and a subfamWHEN
'Current address: Department of Entomology, 410 Forbes Hall, University of Arizona, Tuscon, AZ 85721. international Institute of Entomology (an institute of CAB International), 56 Queen's Gate, London SW7 5JR United Kingdom.
ily of parasitic wasps in the Aphelinidae. In the strepsipteran family Myrmecolacidae males develop as parasitoids of ants, whereas the females that are known have been found to be parasitic on orthopteroids throughout their life (Kathirithamby and Hamilton 1992). Males disperse to find and mate with females, who are embedded between the abdominal sclerites of the orthopteroid host. The distribution of the viviparous offspring then appears to happen passively, as the host moves around in the environment. Although male and female larvae may infect the same ant or orthopteroid, only the larvae of the appropriate sex survive to adulthood (Young 1987). Almost all of the species in the subfamily of aphelinids called the Coccophaginae are heteronomous (Hayat 1985). In almost all of the known cases, females are primary internal parasitoids of immature homopterans such as whitefly or scale insects. Most commonly males develop as hyperparasitoids, that is as obligate parasitoids of developing primary parasitoids of whitefly or scale, often females of their own species. Aphelinid parasitoids with this life history have been called "autoparasitoids," or "heteronomous hyperparasitoids" (Walter 1983a). The haplodiploid genetic system common to all known Hymenoptera (females generally
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
develop from fertilized, diploid eggs and males from unfertilized, haploid eggs) coupled with the ability of mated females to selectively fertilize eggs as they pass through the oviduct, allows male and female eggs to be placed by the female in the correct host. Judged by the relative reluctance of unmated females to oviposit in the homopteran host compared with the hymenopteran host, females seldom make mistakes (Gerling 1966, Williams 1972, Gerling et al. 1987, Hunter 1991). A life history in which females develop as primary parasitoids of homopterans and males develop as hyperparasitoids is almost certainly ancestral to all others in the Coccophaginae. Variation in the mode of male development occurs in several species throughout the lineage, but these exceptional biologies are generally found in only 1 genus. In some species of Coccophagus, both males and females are primary parasitoids, but whereas females develop within the host, males develop externally (Walter 1983b). Perhaps the most extreme specialization described in the literature, however, occurs in the Encarsia, called "heterotrophic" by Walter (1983a), that produce females as primary parasitoids of whitefly and males as primary parasitoids of Lepidoptera eggs. We investigated 1 of these species. The use of the term "heterotrophic" to classify a distinct life history was considered premature by Polaszek (1991) who pointed out that it could not be determined from the literature whether males of these Encarsia species were obligate parasitoids of Lepidoptera eggs, or hyperparasitoids of whitefly that were able to parasitize Lepidoptera eggs facultatively. Most records simply document Encarsia males being reared from Lepidoptera eggs collected in the field. In the most detailed investigation, Beingolea (1959), working in Peru, reared many Encarsia sp. A males from Lepidoptera eggs, but also stated that a few were reared from whitefly as well, although he did not specify whether these few males were primary parasitoids or hyperparasitoids. Encarsia sp. A is likely to have been Encarsia porteri (Mercet), the only South American species known to have this biology (Williams and Polaszek 1996). To clarify this confusion, we investigated the host relationships of Encarsia porteri (Mercet) collected in Argentina. We were particularly interested in discovering whether males of this species develop exclusively on Lepidoptera eggs or may also develop as primary or secondary parasitoids of whitefly. Materials and Methods Collection and Culturing of E. porteri. E. porteri was collected as part of a foreign exploration program for natural enemies of the sweetpotato whitefly, Bemisia tabaci (Gennadius), and the poinsettia whitefly, Bemisia poinsettiae Hempel. During searches in and around Tucuman, Argentina, in February 1994, E. porteri was found to be the
Vol. 89, no. 5
most common parasitoid of Bemisia sp. on soybean. Parasitized Lepidoptera eggs (e.g., velvetbean caterpillar, Anticarsia gemmatalis Hiibner) were also collected and isolated from soybean around Tucuman. Later collections from soybean in Salta Province made by H. Lazaro provided additional female E. porteri for our laboratory cultures. Females and males from the original field collection, and females from the 2nd collection were incorporated in a culture of E. porteri. Females were reared on 2nd through early 4th instars of the sweetpotato whitefly, Bemisia tabaci (strain "B", = B. argentifolii Bellows & Perring), on hibiscus, Hibiscus rosa-sinensis L. Males were reared on eggs of bollworm, Helicoverpa zea (Boddie), that were
