qParasitology INTTZPLt&LYNAL ELSEVIER International Journal for Parasitology 30 (2000) 669-674 PARASITOLOGY www .elsevier.nl/locate/ijpara Controversies in parasitology Parasites and host life-history traits: implications for community ecology and species Co-existence Frédéric Thomas*, Jean-François Guégaii, Yannis Michalakis, Francois Renaud CEPM, UMR CNRS-IRD 9926, 911 Aveiiiie Agropolis B.P.5045, Equipe 'Ei~olutiondes Systèmes Symbiotiques', 34032 Montpellier. cedex I, I ' Frailce Received 7 January 2000; received in revised form 2 March 2000; accepted 3 March 2000 Abstract Most of the evidence for a key role of parasites in structuring communities is based on the idea of a differential susceptibility of host species to infection and its consequences. Recent advances in community ecology suggest that life-history traits of free- living species can be an important determinant of their Co-existence within communities. On the other hand, parasites have the potential to indirectly alter the life-history traits of their hosts, such as developmental time or dispersal. We discuss the idea that these indirect effects could influence the structure of free-living and parasite communities. We explore this idea in relation to related concepts including 'parasitic arbitration' and engineering processes. 0 2000 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. Keyiuords: Community ecology; Life-history traits; Parasites One major goal of community ecology is to identify role in community ecology beyond arbitration. Our the ecological and evolutionary processes which gener- argument is based on three steps: (i) that life-history ate, maintain and erode biological diversity in ecosys- traits of species are important determinants of co-exist- tems [1,2]. For decades the major biotic determinants ence, (ii) that hosts compensate for the negative effects of community structure were assumed to be compe- of infection by altering life-history traits, other than tition and predation. Since the pioneering work of those directly affected by the parasites (e.g. develop- Park [3], however, showing that one parasite with mental rate or dispersal), and (iii) that through their differential effects on two host species can change the potential to alter the life-history traits of their hosts, outcome of competition between these species, ecolo- parasites can influence and significantly alter the struc- gists acknowledged the importance of parasites as a ture of free-living communities. This process is much factor structuring interacting populations within com- more general than arbitration. In arbitration, parasites munities [4-IO]. Mainly because few other ideas have differentially affect the growth of competing host been really explored, ,it is also generally accepted that species. The compensatory modifications of life-history this 'parasitic arbitration' [SI in ecosystems is the main traits, however, potentially allow infected hosts to process through which parasites influence the structure exploit niches , unavailable to uninfected hosts thus of communities. allowing co-existence. First, we briefly review the evi- In this paper, we generalise the idea that parasites dence on the first two steps since extensive reviews on could play an important ecological and evolutionary these topics can be found elsewhere. We then discuss cases where the third step could be observed, and its consequences on the community structure of both * Corresponding author. Tel.: + 33-467-41-6232; fax: + 33-467-41- 6299. hosts and parasites. Such new insights offer useful E-mail address: [email protected] (F. Thomas). ideas and predictions on the influence of parasites on 0020-7519/00/$20.00 0 2000 Australian Society fof Parasitology Inc. Published by El PII: SO 02 O - 7 5 1 9 (OO) O O 040 -0 "J I O O02 1 1479 670 al. F. Thomas et 1International Journal for Parasitology 30 (2000) 669-674 species Co-existence within communities, and thus theoretically favoured by selection if they partly com- deserve consideration both from an ecological and pensate the losses due to the parasite by reproducing evolutionary perspective. earlier [27,28]. In doing so, infected individuals may increase their reproductive activities before dying or being castrated by parasites [3 1-35]. Parasites also 1. Life-history traits and species co-existence have the potential to impose selective pressure on other life-history traits such as growth [36], dispersal Increasingly, ecologists recognise that, in addition to [37-391 or reproductive effort [40,41]. In addition, ecosystem traits (e.g. productivity, compIexity, stabi- when the risk of parasitism is significantly correlated lity. ), organismal traits (e.g. body size, dispersal within families across generations, and when mothers ability, fecundity, timing of reproduction.. ) have a can alter the phenotype of their offspring, there is also strong influence on the Co-existence of species [2]. Evi- evidence for inter-generational modifications of life-his- dence indeed suggests that species with certain life-his- tory traits, i.e. influence of the parental parasite load tory traits are more likely to Co-exist than others. A on the life-history traits of offspring [37]. simple reason for this phenomenon is that different Finally, when the trade-offs between life-history life-history traits may favour resource specialisation, traits and parasite resistance have a genetic basis, para- and then Co-existence based on resource partitioning. site pressure can lead to an evolutionary change in the For instance, morphological differences such as body host population. For instance, hosts living in an en- size among a set of closely related species often consti- vironment where the risk of future infection is high tute the causal basis for the utilisation of different may reduce their age of sexual maturity in order to types of resources which in turn facilitates the co-exist- reproduce before becoming infected [42,43]. ence between these species [l l-141. Similarly, sequen- Thus, parasites are responsible for changes in their tial reproductive periods within a group of species (i.e. host life-history traits by directly manipulating them to temporal segregation) can reduce the possibility and enhance their fitness and/or by inducing adaptive re- magnitude of resource competition [ 15,161. Dispersal is sponse from their host. another important organismal trait in terms of its po- tential to influence species co-existence in both evol- utionary and ecological contexts. Whether a species 3. Parasites, host life-history traits and species co- can successfully colonise new habitats and the poten- existence tial for local adaptation largely depend on its dispersal [17-221. In addition, dispersal has often been identified Several cases of interactions between host life-his- as an important factor which influences the genetic tory traits involved in the Co-existence of host species diversity and the structure of populations, and the and those altered by parasites can be conceived. The probability of regional/global extinction [ 13,23,24]. simplest situation is the case of non-interference when traits altered by parasites do not correspond, or are not related, to the life-history traits involved in host 2. Parasites and host life-history traits species Co-existence. Although cases of non interfer- ence are probably common, life-history traits altered Parasites have been hypothesised to play an import- by parasites can also correspond directly with, or may ant role in the evolution of host life-history traits be related to, life-history traits involved in the co-exist- because they often impose important selective press- ence of species. Several situations previously assigned ures on them. Parasites remove resources from their to ‘parasitic arbitration’ fall within the scope of the hosts that could otherwise be used for host growth, ideas presented here. For instance, numerous parasites maintenance or reproduction [25]. Direct costs result- have the potential to decrease the fecundity and/or the ing from this exploitation are the first cause of survival of their hosts. By altering these two life-his- between-individual or between-population variation in tory traits (through direct effects), parasites can also the life-history traits such as fecundity, growth or sur- alter the population dynamics of their hosts and in- vival. directly the community structure (see references in Alternatively, changes in host life-history traits may introduction). be an ‘adaptive response to parasitism [26]. For However, the alteration of these two life-history instance, one solution developed by many animal traits (i.e. survival and fecundity) by parasites can also species against biotic aggressors (such as parasites) is correspond with negative genetic correlations among the adjustment of life-history traits in order to com- life-history traits (i.e. evolutionary trade-offs) [44,45]. pensate for their negative effects on fitness [27-301. For instance Poiani [46] has shown in a comparative Hosts unable to resist infection by other means (e.g. study that parasitism is associated with small clutch immunological resistance or inducible defences) are size in birds. The interpretation of this relationship is al. (2000) 67 I F. Thoinas et 1Inteiriatioiial Journal foi Parasitology 30 669-674 1 that since parasitisin selects for less investment in each existence [2]. Parasites selecting for early reproduction reproductive event, parasitised