587 REVIEW ARTICLE Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts F. LEFEBVRE and R. POULIN* Department of Zoology, University of Otago, P.O. Box 56 Dunedin, New Zealand (Received 7 September 2004; revised 15 November 2004; accepted 15 November 2004) SUMMARY Precocious egg production, i.e. progenesis, has been documented for a number of species in scattered reports throughout the trematode literature. The last 2 extensive studies on the subject date from Buttner in the early 1950s (in French) and from Tang in the early 1980s (in Chinese). Overall, 43 species were then known for their ability to produce eggs at the metacercarial stage while still in the second intermediate host. Here, we update the list, and document the existence of progenesis in a total of 79 digenean trematode species, for which we provide information on the taxonomy of the hosts, the facultative or obligate character of progenesis, relevant references, as well as some other pertinent biological information. We then review the subject by asking 7 questions of fundamental evolutionary importance. These include: What favours progenetic development? What are the associated costs and benefits? How are progenetic eggs released from the host? While exposing the various opinions of previous authors, we attempt to give a synthetic overview and stress on the importance of the metacercarial cyst wall (whether it is present, and if so its thickness) in the evolution and the adoption of a progenetic life-cycle. Key words: Digenea, life-cycle, metacercariae, reproductive strategies, self-fertilization, egg production. INTRODUCTION that, in neotenic organisms, first reproduction occurs at the same age as in normal organisms, via Precocious egg production in parasites has been the retardation of somatic development. Both these known since the report by von Siebold (1835), processes are thus characterized by the retention of ‘Helminthologische Beitra¨ge’, on eggs released from juvenile characters by adult stages (paedomorphic metacercariae found in the crayfish Astacus astacus. phenotypes; see for example Reilly, Wiley & The term ‘proge´ne`se’, i.e. progenesis later in Meinhardt, 1997). So, basically, progenesis is English, was originally proposed by Giard (1887) for wrongly applied to trematodes, in which precocious sexual maturity of animals that have not yet attained worms are morphologically similar to the adults the adult stage. Dollfus (1924) first applied the term found in the definitive host. However, the term to trematodes when he observed egg production by progenesis is now so widely used in the para- the metacercariae of Pleurogenoides medians sitological literature that it would be pointless and (Pleurogenidae). Now, the concept of progenesis is confusing to introduce a more specific term. We widely employed in palaeontology and botany, and must simply use the term keeping in mind that it quite commonly reported in many animal taxa refers to the attainment of both sexual and somatic (Anura, Urodela, Polychaeta). development in the non-definitive host. In our At present, the accepted definition is the formal view, the most relevant definition for progenesis in one proposed by Gould (1977): any heterochronic trematodes is the production of viable eggs in development in which first reproduction occurs at an individuals inhabiting an organism that would earlier age, i.e. sexual maturation in an organism still normally be considered an intermediate host. in a morphologically juvenile stage. It is often con- Progenesis in trematodes thus encompasses all fused with the term neoteny, but differs from it in cases where a larval stage, a metacercaria or even a cercaria, attains such a degree of maturity that it can produce viable eggs. As a result, the life-cycle may * Corresponding author: Tel: +64 (0)3 479 7983. Fax: +64 (0)3 479 7584. E-mail: robert.poulin@stonebow. be completed in 2 hosts or even in a single host. otago.ac.nz Progenesis may manifest itself in various degrees, Parasitology (2005), 130, 587–605. f 2005 Cambridge University Press doi:10.1017/S0031182004007103 Printed in the United Kingdom F. Lefebvre and R. Poulin 588 from sporadic cases of egg production (1st stage of overview of progenesis, if only for comparative progenesis, according to Buttner, 1955) up to the purposes. Here, we first provide an up-to-date obligate progenetic life-cycle (4th stage of pro- compilation of progenetic trematode species, prior to genesis). In such extreme cases, progenetic metacer- addressing a range of important questions about the cariae are functionally and morphologically similar evolution of progenesis. to adult forms in the definitive host, and are some- times referred to as adults. However, we agree with Grabda-Kazubska (1976), that it is less confusing to TAXONOMIC REVIEW: UPDATING THE LIST keep calling them progenetic metacercariae or pro- genetic forms rather than adults, specifically when Based on 2 previous works (Wu, 1938; Dawes, dealing with the evolution of life-cycles. Similarly, it 1946), Yeh & Wu in 1950 compiled a list of 12 seems to us important and useful to use the term trematode species for which progenesis had been historical host (see Maillard, 1973) to refer to the recorded. The first extensive review, however, was functional host in the ancestral 3-host life-cycle completed by Buttner in 4 consecutive papers (e.g. the historical definitive host). published in French (Buttner, 1950a; 1951a, b, c). Progenesis and abbreviated life-cycles have been This author investigated the biological significance considered previously in the context of life-cycle of progenesis and discussed in detail 30 progenetic evolution in trematodes, but usually as a marginal trematode species. A second species list was phenomenon (Ginetsinskaya, 1988; Galaktionov & later published in Chinese by Tang in 1980. The Dobrovolskij, 2003). Truncated life-cycles have author, mainly referring to the Asian literature, evolved independently many times in the phylogeny compiled a list of 23 progenetic trematode species. of trematodes (Poulin & Cribb, 2002). Progenesis is, So, at the time of this last review, leaving out in fact, only one of many ways in which trematodes duplicates, somewhere around 43 progenetic trema- can abbreviate their complex life-cycle (Grabda- todes were known (i.e. taxa identified to species Kazubska, 1976; Poulin & Cribb, 2002). Basically, level). in addition to progenesis, elimination of 1 or 2 hosts Since then, a significant number of species needs from the life-cycle can be achieved by (i) using the to be added to the list for different reasons: (i) mollusc first intermediate host as the second inter- oversight of progenetic species in the previous lists, mediate host (no historical second host, metacer- (ii) new evidence of progenetic development among cariae encyst in the mollusc and are ingested by a previously described species, (iii) description of vertebrate definitive host), or by (ii) using the mol- new species exhibiting progenetic development, (iv) lusc first intermediate host as second intermediate as revision of the trematode taxonomy. well as definitive hosts (no historical second inter- Excluding blood flukes, we list here 79 trematode mediate and vertebrate hosts, sporocysts directly species for which egg production has been docu- produce either sexual adults or miracidia). However, mented at the metacercarial stage (see Table 1). progenesis is by far the most common way to shorten They belong to 50 genera and 24 families. Some of the life-cycle and 1-host life-cycles are very rare these families appear over-represented in the list; 5 (Poulin & Cribb, 2002). In this review, we focused out of the approximately 100 trematode families only on the possible elimination of the historical currently recognized (see Gibson, Jones & Bray, vertebrate host (i.e. egg production by the meta- 2002) account for more than 50% of the total number cercariae in the historical second intermediate host). of progenetic species listed here (Allocreadiidae We thus restricted our synthesis to trematodes for N=9; Hemiuridae N=6; Macroderoididae N=11; which a cercarial stage penetrates, then matures into Microphallidae N=6; Opecoelidae N=9). Among a metacercarial stage and produces eggs in a second these families, the genus Alloglossidium (Macro- intermediate host. We only investigated the subclass deroididae) is particularly remarkable with a total of Digenea, with no regard to the small sister group 11 progenetic species. Aquatic invertebrates are the Aspidogastrea. Moreover, it must be pointed out historical second hosts of most progenetic trema- that we did not consider in our taxonomic review the todes (crustaceans N=47; insects N=14; leeches species belonging to families for which all members N=8; molluscs N=7; polychaetes N=1), though are progenetic, i.e. the blood flukes Sanguinicolidae, vertebrates are not rare (fish N=14; amphibians Spirorchidae, and Schistosomatidae. They represent N=8). Concerning the definitive hosts, most of an ancestral life-cycle truncation inherited by all them are fish in case of facultative progenesis (fish species in the clade, and are therefore much more N=45; amphibians N=7; mammals N=6; reptiles specialized for a 2-host cycle than other taxa. N=5; birds N=4). Overall, obligate progenetic Accounts of the biology and epidemiology of these 3 species (i.e. with no demonstrated definitive host) families and other relevant information can be found represent 26% of progenetic species for which we elsewhere in the literature. Nonetheless, because have information on this aspect (obligate progenetic they represent a major transition in trematode evol- species: N=17; facultative progenetic species: ution, we consider blood flukes in our synthetic N=48). Progenesis in trematodes 589 BIOLOGICAL REVIEW: QUESTIONS AND ANSWERS lineages. Recent investigations using analysis of Throughout the last century, many evolutionary character convergence strongly support the idea that aspects of progenesis in trematodes have been the the 2-host life-cycle derived from a more ancient subjects of fruitful debates.