Parasitol Res (2003) 89: 81–88 DOI 10.1007/s00436-002-0638-z

ORIGINAL PAPER

S. Trouve´Æ S. Morand Æ C. Gabrion Asexual multiplication of larval parasitic worms: a predictor of adult life-history traits in Taeniidae?

Received: 16 December 2001 / Accepted: 22 January 2002 / Published online: 3 September 2002 Ó Springer-Verlag 2002

Abstract The hypothesis that asexual multiplication and discussed in the context of host-parasite interac- inside the intermediate host and adult life-history tions. traits within the final host are independent is tested among Cestoda. Using phylogenetic relationships among the Cestoda species, we can show that asexual multiplication appears to have been lost and recovered Introduction several times throughout Taeniidae evolution; this al- lows a comparison of the adult life-history traits of Indirect life-cycles (i.e. when the parasitic species needs species with and without asexual multiplication at the several hosts to achieve its development) have evolved larval stage. The adult trait considered is the size of independently in several parasitic taxa and appear pre- the parasite, since numerous life-history traits, such as dominant in host-parasite systems (Morand 1996). This fecundity and longevity, are correlated with size. If is especially true when only metazoans are considered. adult traits are independent of whether the larval stage In groups exhibiting parasitism as a mode of life, such as reproduced asexually or not, we expect no difference cestodes, digeneans, acanthocephalans and nematodes, in the adult size of the proliferative (i.e. with asexual at least 65% of the species have an indirect life-cycle multiplication) and non-proliferative species. The re- (Morand 1996). Indirect life-cycles differ from simple sults are inconsistent with this hypothesis. In contrast, life-cycles in a number of ways. For instance, it has been species with asexual multiplication in the intermediate noted that indirect life-cycles may allow the appearance host seem to have smaller adult size, reflecting a trade- of two ‘‘generations’’: a sexual one occurring within the off. We propose that ecological factors involving in- final host and an asexual one in the intermediate host. traspecific and interspecific competition in the final Asexual multiplication within the intermediate host ap- host might be responsible for this trade-off. The role pears as a characteristic in some groups of platyhel- of these parameters in the evolution of life-history minthes (digeneans), whereas it does not represent an traits and more precisely in the acquisition of asexual invariant part of cestode life-cycles. The unequal re- multiplication is investigated with comparative analysis partition of asexual multiplication is a question that has long intrigued biologists. Several explanations have been proposed to explain the adaptive benefits of asexual multiplication in para- S. Trouve´ sitic organisms. These explanations include (1) the Laboratoire Ecologie-Evolution, UMR CNRS 5561 Bioge´ osciences, 6 Bd Gabriel, maintenance of gene complexes adapted to the infesta- Universite´ de Bourgogne, 21000 Dijon, France tion, and development inside the host (Williams 1975; Price 1977); (2) a weakened intermediate host, favouring S. Morand (&) Centre de Biologie et d’Ecologie Tropicale et Me´ diterrane´ enne, host-to-host transmission (Moore 1981). Certainly the Laboratoire de Biologie Animale, UMR 5555 du CNRS, most widely mentioned explanation is (3) that asexual Universite´ de Perpignan, Av. de Villeneuve, multiplication would allow the production of a new 66860 Perpignan Cedex, France source of proliferation (Price 1977, 1980) while exploit- E-mail: [email protected] Fax: . +33-4-68662281 ing two different environments to reproduce, the inter- mediate and the final host. This hypothesis has been C. Gabrion Laboratoire d’Ecologie Evolutive Parasitaire UMR 7103 CNRS, further developed. Moore (1981) and Loker (1983) even Universite´ Pierre et Marie Curie, CC 175, proposed that a low rate of reproduction in one host 7 quai St. Bernard, 75252 Paris Cedex, France could be compensated by proliferation in the other host. 82 This suggests the existence of a trade-off between asex- expect a positive association between species richness and ual multiplication within the intermediate host and the occurrence of asexual multiplication. The role of sexual reproduction in the final host. In other words, these two ecological determinants (intra- and interspec- life-history traits of the larval and adult parasitic stages ific competition) in the acquisition of asexual multipli- would not be independent. However, this explanation is cation is investigated through comparative analyses. far from evident and needs relevant statistical analysis to test it. As related species share many characters through common descent, they generally cannot be considered as Materials and methods independent data points in statistical analysis. One way to solve this problem is to use a comparative method The data (Fig. 1) on which we based our analysis comprised 20 with controls for the effect of phylogenetic associations species of Cyclophyllidea (Platyhelminthes, Cestoda) including 17 species of the genus Taenia, two species of the genus Echinococcus (Felsenstein 1985; Garland et al. 1992). and one species of the genus Cladotaenia. The last three species Through the present study, we tested the existence of were included to act as an outgroup when mapping the presence/ a trade-off between asexual multiplication inside the absence of asexual multiplication on the phylogeny. Like most intermediate host and life-history traits within the final platyhelminthes, Cyclophyllidea species are simultaneously her- host and we used controls for the effect of phylogenetic maphroditic. Their life-cycle is heteroxenous, with sexual repro- duction in the final host that can be preceded by asexual association. For this purpose we studied the Cestoda, in multiplication in the intermediate host. which metacestode proliferation is only known in about The life-history traits recorded for each parasitic species were 20 species and six cestode families with approximately (Tables 1, 2): half occurring in the family Taeniidae (Whitfield and 1. Worm length: the length of the adult stage (mm). Evans 1983). 2. Presence or absence of asexual multiplication in the intermediate First, we mapped the asexual multiplication onto the host. phylogeny of Cestoda. This showed that this character has evolved independently several times throughout Taeniidae diversification. Therefore, the Taeniidae con- stitute a valuable group to test our hypothesis. Secondly, we investigated the relationship between adult life-history traits and asexual multiplication. The adult trait considered was body size, since it is com- monly known that in parasites, as well as in free-living organisms, size determines numerous life-history traits, notably egg production (Skørping et al. 1991; Roff 1992; Stearns 1992; Charnov 1993; Poulin 1995; Morand and Sorci 1998; Trouve´ et al. 1998; Trouve´ and Morand 1998). The results suggest that species with asexual multiplication in the intermediate host present smaller adult size, reflecting a trade-off. As a third point, the reproductive trade-off between final and intermediate hosts allows the hypothesis on the evolution of asexual multiplication to be tested. Two main ecological factors, i.e. intra- and interspecific competition, could explain the reduction in adult size in the proliferative species. Indeed, asexual multiplication at the larval stage might result in higher worm intensity within the final host, generating intraspecific competi- tion. Since intraspecific competition often induces a re- duction in adult body size, we expect a negative relationship between adult parasite size and the intensity of infection. If this is the case intraspecific competition might have favoured the evolution of asexual multipli- cation to compensate for the loss of reproductive success due to smaller adult size in the final host. Such a role could also have been played by interspecific competition resulting from high parasite richness within the final host. Fig. 1 Working phylogeny of the Cestoda used to investigate life- As interspecific competition is expected to result in a history covariations. This supertree, compiled from three phyloge- reduction in adult worm size and thus egg production, it netic trees (Moore and Brooks 1987; Okamato et al. 1995; de Queiroz and Alkire 1998), has been elaborated following the basic might select for asexual multiplication within the inter- algorithm of matrix representation with parsimony using the mediate host to compensate for the decrease in repro- PAUP program. Colours refer to the presence or absence of ductive success in the final host. In this case we would asexual multiplication 83

Table 1 List of cestode species with length and presence/absence of asexual multiplication (respectively coded as 1/0) and epidemiological data Cestode species Length Asexual Intensity Mean intensity Host species References (mm) multiplication (mini-maxi) (mini-maxi)

Echinococcus granulosus 8 1 126,000 810 Canis lupus Samuel et al. 1978 E. oligarthrus 31 – – Taenia endothoracicus 350 1 20 – Vulpes vulpes T. multiceps 700 1 472 32,2 Canis latrans Pence and Windberg 1984 T. brauni 420 1 62 – T. cervi 210 0 – T. crassiceps 220 1 41–256 0–30 Canis spp. Samuel et al. 1978; Seesee et al. 1983 T. hydatigena 5,000 0 9 5.5 Canis lupus Samuel et al. 1978 T. martis 100 0 4,0–5 0 Bassariscus astutus, Pence and Willis 1978; Martes americana Hoberg et al. 1990 T. mustelae 100 1 12,0–38 1.0–5.5 Mustela vison, Miller and Hakerma 1964; Martes americana Jennings et al. 1982; Poole et al. 1983 T. omissa 600 0 246 47 Felis concolor Waid and Pence 1988 T. ovis 1,000 0 – – T. pisiformis 1800 0 83–200 9.0–19 Canis spp., V. vulpes Samuel et al. 1978; Dibble et al. 1983; Seesee et al. 1983; van den Bussche 1987 T. rileyi 640 0 25–154 4.2–81 Felis canadensis, F. rufus Stone and Pence 1978 T. selousi 55 1 – – – T. serialis 700 1 100 21 Canis latrans Pence and Meinzer 1979 T. taeniaeformis 60 0 91 – Felis cati T. taxidiensis 480 0 4 4 Taxidea taxus Seesee et al. 1983 T. twitchelli 210 1 61 17 Gulo gulo Rausch 1959

Table 2 Richness of cestode species in carnivore species (data from controlled for host sampling size (ln-transformed) and the residuals Morand and Poulin 1998) were used in the subsequent analysis. To control for phylogenetic effects we constructed a working Host species Host Cestode Host body phylogeny for the parasitic species (Fig. 1) compiled from three sampling size species richness weight (kg) phylogenetic trees provided by Moore and Brooks (1987), Okamoto et al. (1995) and de Queiroz and Alkire (1998). Moore Alopex lagopus 38 3 5.5 and Brooks (1987) investigated the relationship between platy- Canis latrans 752 10 16 helminthes using morphological data whereas Okamoto et al. Canis lupus 266 10 43 (1995) and de Queiroz and Alkire (1998) used cytochrome c oxi- Vulpes vulpes 238 8 5 dase and the combined data of cytochrome c oxidase and 28 s Felis canadensis 360 5 15 rDNA, respectively. A supertree was developed following the basic Felis concolor 99 2 110 algorithm of matrix representation with parsimony (MRP: Ragan Felis silvestris 71 5 10 1992; Sanderson et al. 1998) using the PAUP program. We also Lynx pardinus 84 25used the phylogenetic hypothesis of Hoberg et al. (2001) based on Lynx canadensis 300 5 10.2 morphological characters. However, two species were not included Martes americana 217 3 1.06 (Taenia cervi and Taenia brauni) and the phylogenetic tree is less Martes pennanti 36 1 4.80 resolved. Data on the host phylogeny (Fig. 2) was obtained from Martes martes 42 1 1.60 several sources (references in Morand and Harvey 2000). Controls Martes foina 305 1 2.30 for the effects of phylogenetic associations were performed using Mustela erminea 62 2 0.11 the independent contrasts method (Felsenstein 1985; Burt 1989) Mustela vison 50 0 0.66 and processed with the CAIC program (Purvis and Rambaut Mustela nivalis 227 0 0.15 1994, 1995). Least squares regression analysis was conducted to Mustela putorius 99 1 1.7 analyse associations between life-history traits across species. All Mustela lutreola 12 0 0.9 regressions between contrasts were forced through the origin (see Taxidea taxus 30 0 10 Garland et al. 1992 for justification). In order to test the phylo- Genetta genetta 283 5 2.2 genetic effect, the analyses were also performed on uncontrolled data.

3. Maximum worm intensity in the final host. 4. Host body size: the weight of the adult (kg) or the average weight when the cestode species parasitizes several host spe- Results cies. 5. Global cestode richness in the final host, which corresponds to the richness across all known hosts of each parasite spe- The asexual multiplication character has been mapped cies. onto the de Queiroz and Alkire’s molecular phylogeny (Fig. 3, which involves a subset of species). The results To standardize residuals, worm length, host body size, maxi- mum worm intensity and host sampling size were ln-transformed, suggest several parallel changes in life-histories: asexual and cestode richness was ln+1-transformed prior to analysis multiplication in the intermediate host has been lost (Harvey 1982). Parasite species richness (ln+1-transformed) was and recovered several times throughout Taeniidae 84

Fig. 2 Phylogeny of carnivores. The value of the species richness in the ancestors of the Canidae, Mustelidae and Felidae is given in bold diversification. Two equally parsimonious hypotheses can give an account of the evolution of this character. If asexual multiplication is ancestral for Taenia, then this adaptation was lost at least twice, once at the emergence of the large clade including T. solium, T. ovis, T. sagi- nata, T. asiatica, T. multiceps and T. hydatigena, and once at the emergence of the clade including T. tae- niaeformis and T. macrocystis (Fig. 3A). This hypothesis implies that asexual multiplication has evolved once within the species T. multiceps. The second hypothesis also supports three major changes in larval form, in- cluding one loss of asexual multiplication in the large clade including T. solium, T. ovis, T. saginata, T. asiat- ica, T. multiceps, T. hydatigena, T. pisiformis, T. tae- niaeformis and T. macrocystis, and two parallel Fig. 3 Asexual multiplication is considered as A a plesiomorphy appearances of this character within the species for Taenia,orB as a synapomorphy T. multiceps and T. pisiformis (Fig. 3B). A significant positive relationship between host body size and worm length for cross-species data (i.e. without parasite phylogeny, the relationship between host body correction for phylogenetic effects: r2=0.48, P=0.002, size and cestode length remains significant: using the Fig. 4A) was found. This relationship may be dubious, supertree (r2=0.32, P=0.0211: Fig. 4B) or using the resulting from the fact that related species are more tree of Hoberg et al. (2001) (n=9; r2=0.54, P=0.0157). likely to share many morphological characters, such as The occurrence of asexual multiplication in the in- length, and are more likely to infect hosts presenting termediate host does not seem to influence adult worm similar size. However when data are controlled for size (controlled for host body size) in the final host when 85 data was not corrected for phylogeny (ANCOVA we regressed worm length on host body size and com- F(1,14)=1.71; P=0.212). The independent contrast puted the residuals. These residuals were then regressed method provides only two contrasts in the reproductive on the residuals of the regression of worm intensity on mode (acquisition versus loss of the asexual multiplica- host body size. The slope of the regression was negative tion) using the phylogenetic tree of Hoberg et al. (2001), but not statistically significant (r2=0.005, P=0.82). which renders a statistical test impossible. The inde- Using independent contrasts, we also found no signifi- pendent contrast method provides five contrasts in the cant relationship using the supertree (r2=0.18, P=0.17: reproductive mode (acquisition versus loss of the asexual Fig. 5). No relationship was found either using Hoberg multiplication) using the supertree (Fig. 1). When the et al.’s phylogenetic tree (n=6, r2=0.04, P=0.66). host size is controlled for, four of these five contrasts are Intraspecific competition does not seem to influence negative, meaning a lower parasite adult size in prolif- parasite adult size. erative species. Although these results cannot be statis- If interspecific competition decreases adult worm size, tically tested, they suggest that asexual multiplication is it might select for asexual multiplication within the in- associated with a decrease in adult body size. This result termediate host to compensate for the decrease in egg could be explained by either intraspecific or interspecific production due to smaller adult size. Thus a positive competition within the final host. The relevance of both association between species richness and the occurrence of these ecological determinants is now discussed. of asexual multiplication is expected. We investigated If intraspecific competition explains the reduction in the cestode species richness within the carnivores, since worm length, we would expect a negative relationship carnivores constitute a predominant percentage of hosts between worm length and worm intensity. To test this, of the Taeniidae. The phylogeny of carnivores (Fig. 2) allows specific richness values (corrected for sampling effort) to be calculated for the ancestors using the CAIC program (Purvis and Rambaut 1995). The highest spe- cies richness is clearly observed in Canidae, whereas the lowest is observed in Mustelidae. The Felidae present an intermediate value (Fig. 2). A Fisher’s exact test re- vealed a significant association between the presence of asexual multiplication and its occurrence in hosts of the family Canidae (P=0.036).

Discussion

For the parasite, the host constitutes not only its habitat but also a source of nutrients and a means of transport. In this context, hosts may be considered to be the major environment in which parasites have evolved and be- come adapted. Due to this coadaptation between hosts and parasites, we expect covariation between parasite and host life-histories (Sorci et al. 1997; Morand and

Fig. 4 Relationship between host body size and worm length. Slopes have been estimated using A ordinary regression (i.e. nonphylogenetic analyses) and B phylogenetically independent contrast analyses. (The relationship remains significant when the Fig. 5 Scatter plot between contrasts of worm length and worm point on the right is removed) intensity. Both variables have been controlled for host body size 86 Sorci 1998; Morand and Poulin 2000). Our finding that dynamics. In the study of Trouve´ et al. 1998) digeneans, host and parasite body sizes are correlated supports this which represent the group with asexual multiplication hypothesis. This same relationship has previously been were compared to tapeworms for which most of the demonstrated in numerous other taxa, such as nema- species considered in the study reproduced without todes (Harvey and Keymer 1991; Morand et al. 1996; asexual multiplication. The present study focused on a Sorci et al. 1997; Morand and Sorci 1998), monogeneans given cestode group, and compared species with and (Sasal et al. 1999), digeneans (Poulin 1997), crustaceans without asexual multiplication. The main difference be- (Poulin and Hamilton 1997) and lice (Morand et al. tween digeneans and tapeworms is that in the latter 2000). group the products of the asexual multiplication remain Beside host adult size, other biological or ecological inside the intermediate host until it is eaten by the final traits can potentially determine the adult life-history host. In digeneans, the larvae produced through asexual traits of parasites. It has been said that asexual multi- multiplication constitute a free-living stage that is re- plication within the intermediate host might be one of leased outside of the intermediate host. Whereas in them (Moore 1981; Loker 1983). Since asexual multi- cestodes the probability that the final host ingests all the plication in Taeniidae seems to have evolved through larvae produced through asexual multiplication is very several independent and parallel appearances and losses high, in the case of digeneans this probability is low. (Fig. 3), we can use this group to seek explanations to Therefore we might expect that in the cestode prolifer- aid our understanding of its role in life-history evolution ative species there is a high worm intensity in the final of parasitic organisms. host. The limited amount of data on infection intensity Our results suggest that proliferative species present a (only three independent contrasts could be computed) smaller adult size compared to the non-proliferative prevents us from testing the interaction between parasite forms. Although this comparison involves only a few intensity and the presence versus absence of asexual independent contrasts, this result is in accordance with multiplication. However, if intraspecific competition previous work done by Moore (1981) and Loker (1983) plays a role in the evolution of asexual multiplication we without controlling for the effect of phylogenetic asso- should observe a negative relationship between infection ciation. Moore (1981) mentioned that in cestodes asexual intensity and life-history traits such as adult size and multiplication is usually associated with small adult size, fecundity. We found no significant relationship between high mortality and low life-time fecundity. Similarly, in adult size and infection intensity, suggesting that the schistosomes, Loker (1983) pointed out a trade-off be- effect of intensity on adult life-histories is negligible. tween reproduction in the final host and asexual multi- This result might be surprising since a large body of plication in the intermediate host and, respectively, ecological literature shows an effect of infection intensity estimated the number of eggs and cercariae produced. In on life-history traits. For instance, body size, ovary size combination with the results from our study, these results and fecundity of the digenean Echinostoma caproni ex- tend to show that the development of the parasite inside hibit a significant decrease with parasite intensity the final host may be closely related with asexual multi- (Christensen et al. 1990; Trouve´ et al. 1999). Moreover, plication inside the intermediate host. Consequently, it has been shown that establishment, growth, egg pro- asexual multiplication would constitute one of the de- duction and survival constitute the life-history traits terminants of the life-history traits of the adult stage. sensitive to density in a broad array of parasitic taxa, This interpretation is in disagreement with the hy- such as cestodes (Keymer et al. 1983), acanthocepha- pothesis proposed by Trouve´ et al. (1998). These authors leans (Ewald and Nickol 1989; Crompton et al. 1988) notably compared digenean species presenting asexual and nematodes (Adamson et al. 1992). multiplication in the intermediate host and cestode In addition to intraspecific competition, interspecific species, most without asexual multiplication, in this competition can also trigger the evolution of living analysis. They showed that when body size is controlled, forms. Although infections of one host by several par- digeneans (with asexual multiplication) and cestodes asite species can, in some cases, facilitate the parasite (mostly without asexual multiplication in that study) establishment through interactions with the host im- have roughly the same reproductive output in the final mune system (Poulin 1998), concurrent infections are host. This suggests that asexual multiplication in the more frequently shown to decrease parasite fitness. intermediate host does not seem to affect the reproduc- Interspecific competition may induce site segregation tive potential in the final host. According to this hy- inside the host (i.e. character displacement), reduce es- pothesis, the intermediate and the final hosts would tablishment probability, and fecundity (Dobson 1985; constitute two environments that are independent from Holmes 1973; Fried and Gainsburg 1980; Andreassen one another in terms of the resources exploited by the et al. 1990; Adamson and Noble 1993). For instance, parasites. In contrast, our results suggest a trade-off Silver et al. (1980) pointed out that the modification of between the asexual multiplication in the intermediate the niche by Trichinella spiralis caused a decrease in host and the life-history traits, estimated by the adult fecundity and the adult size of Hymenolepis diminuta size, inside the final host. when both species were present in rat intestine. Fol- Nevertheless this inconsistency may only be apparent, lowing a primary infection with Nippostrongylus brasil- and may be caused by a difference in transmission iensis, metacercariae of Echinostoma caproni and 87 Echinostoma trivolvis are expelled from the mouse (Trematoda). Infections in hamsters and jirds. J Helminthol Soc intestine (Fujino et al. 1996). Wash 57:104–107 Crompton DWT, Arnold SE, Walters DE, Keymer AE, Marris In the context of our study, interspecific competition RW (1988) Factors influencing the fecundity of Moniliformis resulting from high parasite richness could have shaped moniliformis acanthocephala constant diet and varied dose. cestode life-histories by significantly reducing adult body J Zool (Lond) 214:313–324 size and decreasing fecundity. In such a case, asexual De Queiroz A, Alkire NL (1998) The phylogenetic placement of Taenia cestodes that parasitize humans. 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