Sexually Transmitted Parasites and Sexual Selection in the Milkweed Leaf Beetle, Labidomera Cli7icollis
Total Page：16
File Type：pdf, Size：1020Kb
OIKOS 92: 91–100. Copenhagen 2001 Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera cli7icollis Patrick Abbot and Larry M. Dill Abbot, P. and Dill, L. M. 2001. Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera cli6icollis. – Oikos 92: 91–100. Milkweed leaf beetles (MLBs; Labidomera cli6icollis Chrysomelidae) are parasitized by a subelytral mite, Chrysomelobia labidomerae (Tarsonemina: Podapolipidae). We show that C. labidomerae is transmitted between MLBs when they copulate, and can reduce the survival of nutritionally stressed beetles. We investigated the effect of this sexually transmitted parasite on mate choice and male-male competition in MLBs, and the consequences of variation in these behaviours for mite transmission. We found no evidence of parasite avoidance by MLBs, and evidence for high rates of parasitism in the MLB populations we surveyed. In the absence of females, para- sitized males contacted unparasitized males more often and for longer than controls, and they tended to displace rival males from females more often than did unpara- sitized males, a result consistent with the interpretation that parasitized beetles compensate for loss of fitness by increasing reproductive effort. These changes can also benefit mites, because longer and possibly more contacts between beetles provide more opportunities for transmission, but there is no evidence that these changes in male behaviour result from parasite manipulation. P. Abbot and L. M. Dill, Beha6ioural Ecology Research Group, Dept of Biological Sciences, Simon Fraser Uni6., Burnaby, BC, Canada V5A 1S6(present address of PA: Dept of Ecology and E6olutionary Biology, Uni6. of Arizona, Tucson, AZ 85721, USA [[email protected]]). Because they require close proximity between hosts for tion is how the effects of disease (or risk of disease) on transmission, infectious diseases can play decisive roles host interactions influence the population biology of in the sexual and social behaviour of their hosts. In the parasites themselves (Møller 1996, Knell 1999). For recent years both conceptual and empirical research example, from the perspective of a contagious parasite, have grown to incorporate the fact that infectious any host behaviours which alter the frequency of con- parasites, especially sexually transmitted parasites, may tacts between parasitized and unparasitized hosts can be common, if cryptic, factors shaping the mating reduce the rate of infectious spread through the host biology of many organisms (Loehle 1995, Lockhart et population, and potentially depress the growth rate of al. 1996). A number of studies have emphasized the the parasite population. For harmful parasites, such various effects of infectious diseases on both host sec- host behaviours may occur commonly: unparasitized ondary sexual characteristics (e.g., Knell 1999) and hosts may avoid parasitized mates, for example, or mate choice (e.g., Able 1996, Loehle 1997, Kiesecker et parasitized hosts may exhibit less competitive ability al. 1999), as well as the direct effects of parasitism on than unparasitized counterparts, reducing the frequency host competitive ability, life history trade-offs, and of direct interactions with other hosts (Loehle 1995, reproductive effort (e.g., Forbes 1991, 1993, Polak and Zuk and McKean 1996). Markow 1995, Thomas et al. 1999). An aspect of the Infectious parasites and their hosts thus can provide interaction that has received comparatively less atten- unique opportunities to explore reciprocal interactions Accepted 15 August 2000 Copyright © OIKOS 2001 ISSN 0030-1299 Printed in Ireland – all rights reserved OIKOS 92:1 (2001) 91 between host behaviour and parasite population biol- Baker and Eickwort (1975) reported an average of 11 ogy (Richner 1998, Clayton et al. 1999). Little empirical mites per beetle in the field, with laboratory densities evidence exists, however, that addresses the extent to ranging as high as 194 mites per beetle. Previous studies which an infectious disease influences host sexual be- have suggested that transmission occurs only by direct haviour, in conjunction with the extent to which those contact between adult beetles: before transmission, host sexual behaviours affect parasite transmission. adult female mites typically move from beneath the Here we consider the joint effects of mate choice and elytra to the abdomen of MLBs and migrate to new male-male competition on the transmission biology of a hosts either during copulation or occasionally during sexually transmitted parasite and simultaneously ask interactions between host individuals of the same sex how the parasites affect these same behaviours. (fighting, for example; Baker and Eickwort 1975, We investigated mate choice and male-male competi- Drummand et al. 1988). Results concerning how the tion for females in the milkweed leaf beetle (MLB) parasite affects survival have been more equivocal Labidomera cli6icollis, parasitized by the mite (Eickwort and Eickwort 1986, Drummand et al. 1989). Chrysomelobia labidomerae Eickwort (Acari: Tarsonem- We investigated sexual transmission by C. ina: Podapolipidae). MLBs occur on milkweed (Ascle- labidomerae and measured MLB survival under para- pias spp. and Cynanchum spp.) throughout the eastern sitism experimentally. We then asked if and how para- U.S. and Canada. Like many chrysomelid beetles, sitism influences the sexual behaviour of beetles by MLBs are characterized by multiple matings, prolonged measuring the effect of mites on mate choice and pairing between males and females, and mixed pater- male-male competition. In the mate choice experiments, nity broods (Dickinson 1986, 1988, 1992, 1997). MLBs we anticipated that unparasitized mates would avoid typically experience only one long season (May–Sep- infectious partners to minimize the likelihood of receiv- tember) favourable to reproduction, in which two or ing parasites (Able 1996, Loehle 1997). In the experi- three overlapping generations are produced. Males ments on male-male competition, the most competitively search for and monopolize females straight-forward expectation was that, because mites (‘scramble competition polygyny’; Dickinson 1992), of- feed on male haemolymph, parasitized males would be ten foregoing feeding to do so, and assure paternity by less competitive than their unparasitized counterparts guarding females until oviposition, and at times insemi- (Siva-Jothy and Plaistow 1999, Thomas et al. 1999). nating females repeatedly. Once a male encounters a However, the range of possible direct effects of para- female, there is little or no courtship before mating. sites on host behaviour extends beyond the pathologi- Male MLBs occasionally fight one another, normally cal, and includes functional changes that benefit hosts, when a solitary male attempts to displace a copulating parasites, or both (Moore and Gotelli 1990, Poulin et male, but fights sometimes occur in the absence of al. 1994, Lafferty 1999). In particular, we bore in mind females, possibly to evict rivals from plants. the possibility that male MLBs may express some de- The family Podapolipidae consists of highly special- gree of functional plasticity in competitive behaviour, ized insect parasites that feed on their hosts by piercing as a means to compensate for the loss of fitness due to the cuticle with their styliform chelicerae (Baker and parasitism (Forbes 1993). In order to identify such Eickwort 1975, Hurst et al. 1995). C. labidomerae is a plasticity (should it occur), we paid particular attention subelytral beetle parasite first described on New York to those effects that altered the outcome of competi- state MLBs (Eickwort 1975). C. labidomerae has since tion, because these are relevant to both parasitized male been described on Labidomera spp. throughout North fitness and to mite transmission opportunities. America, and morphologically-indistinguishable species Finally, after measuring the effect of the parasite on of mites have been described on Leptinotarsa spp. over MLBs, we asked if variation in parasite transmission is the same range. potentially correlated with the observed variation in Female C. labidomerae lay eggs on the wings of the host sexual behaviour, and if mite prevalence in a wild host, laying on average 1–2 eggs per day (Baker and population is consistent with the observed host Eickwort 1975, Drummand et al. 1988). Larvae mature behaviours. at the base of the wings or in the thoracic crevice, where they feed (Regenfuss 1972). The engorged nymphs then migrate to the ventral surface of the elytra, and develop into adults. Adult females overwin- Methods ter under the elytra of diapausing adult beetles, appar- Laboratory methods ently synchronizing their diapause to match that of their hosts (Baker and Eickwort 1975, Drummand et al. Approximately 250 milkweed leaf beetles were collected 1988). With no free-living stage, C. labidomerae cannot from the Queen’s University Biological Station at El- survive off their host for more than a few minutes to a gin, Ontario, Canada (44°34% N, 76°19% W), and from few hours, and mite numbers can grow quite large the Cornell Biological Field Station near Bridgeport, (Baker and Eickwort 1975, Drummand et al. 1989). New York, USA (43°09% N, 75°58% W). Asclepias and 92 OIKOS 92:1 (2001) beetles were locally abundant at both field sites. We To measure the effect of mites on starved beetles, we bred beetles from both populations in the laboratory, selected 36 two-month-old