Resolving evolutionary changes in parasite life cycle complexity: Molecular phylogeny of the trematode genus Alloglossidium indicates more than one origin of precociousness.

The evolutionary causes and consequences of changes in complex life cycles are of central importance in parasitology. However, data remain limited because in part, knowledge on phylogenetic relationships among species that differ in life cycle patterns remains scarce. We present a molecular phylogeny of the trematode genus Alloglossidium, which contains several species that display precocious (a.k.a., progenetic) life cycles (i.e., maturation in what is typically regarded as an intermediate host). The molecular phylogeny contrasts with previous morphological and life-history based phylogenetic hypotheses. In particular, a precocious life cycle wherein leeches are used as final hosts evolved early in the history of the genus. Among the remaining species, which are a separate clade, a three-host life cycle using ictalurid catfishes is ancestral. Furthermore, there are at least two additional independent evolutionary events that lead to a precocious life cycle where a catfish host is lost and a crustacean is used as a final host. We conclude with a discussion on how existing hypotheses on the evolution of precociousness, and parasite life cycle complexity in general, may or may not relate to the patterns observed in genus Alloglossidium.

Evolutionary consequence of a change in life cycle complexity: A link between precocious development and evolution toward female-biased sex allocation in a hermaphroditic parasite.

The evolutionary consequences of changes in the complex life cycles of parasites are not limited to the traits that directly affect transmission. For instance, mating systems that are altered due to precocious sexual maturation in what is typically regarded as an intermediate host may impact opportunities for outcrossing. In turn, reproductive traits may evolve to optimize sex allocation. Here, we test the hypothesis that sex allocation evolved toward a more female-biased function in populations of the hermaphroditic digenean trematode Alloglossidium progeneticum that can precociously reproduce in their second hosts. In these precocious populations, parasites are forced to self-fertilize as they remain encysted in their second hosts. In contrast, parasites in obligate three-host populations have more opportunities to outcross in their third host. We found strong support that in populations with precocious development, allocation to male resources was greatly reduced. We also identified a potential phenotypically plastic response in a body size sex allocation relationship that may be driven by the competition for mates. These results emphasize how changes in life cycle patterns that alter mating systems can impact the evolution of reproductive traits in parasites.

Alloglossidium floridense n. sp. (Digenea: Macroderoididae) from a spring run in North Central Florida.

A new species of Alloglossidium is described from the intestines of 2 madtom species (Noturus leptacanthus and Noturus gyrinus) that were collected from the run of a small, unnamed spring system that drains into the Santa Fe River, Florida. Alloglossidium floridense n. sp. is morphologically very similar to other nonprecocious Alloglossidium spp. that use ictalurids as definitive hosts, but can be distinguished by a combination of its smaller overall size (length and width), large eggs in relation to its small body size, position of the vitellaria, ovary shape, and position of the ovary in relation to the cirrus sac. A comparison of nuclear rDNA sequences (spanning partial 18s, complete ITS1, 5.8s, ITS2, and partial 28s regions) showed that A. floridense n. sp. diverged by 0.70-3.17% from the other 4, nonprecocious species that infect ictalurids (Alloglossidium corti, Alloglossidium fonti, Alloglossidium geminum, and Alloglossidium kenti). The new species of Alloglossidium, described herein, is the first of the genus to be reported from Florida and the first to be recorded from N. leptacanthus . In light of the subtle morphological differences among the nonprecocious species that infect ictalurids, we discuss how previous descriptions of species traits that are not supported with genetic data are difficult to interpret because of the possible past nonrecognition of distinct species.

Interaction of two myxozoan parasites from naked goby Gobiosoma bosc, in Lake Pontchartrain, Louisiana.

During a parasitological survey of naked gobies ( Gobiosoma bosc ) in Lake Pontchartrain, Louisiana, U.S.A., 2 myxozoan parasites were found infecting the gall bladders of 84 of 90 fish. Parasite plasmodia of each were morphologically distinct; plasmodia bearing Ellipsomyxa-like spores were elongate and fusiform (1,126 by 403 µm), and those bearing Sphaeromyxa-like spores were large and discoid (1,400 µm diameter). Neither parasite conformed to any described species of myxozoan, and both are described here. Sphaeromyxa kenti n. sp. bears boomerang-shaped spores ranging 17.5-19.8 µm long by 3.8-5.2 µm wide. Two unequal sized polar capsules contain ribbon-like polar filaments characteristic of this genus. Ellipsomyxa adlardi n. sp. bears ovoid spores 11.3-14.4 by 7.1-8.8 µm, with 2 rounded polar capsules oriented in opposite directions relative to the longitudinal plane of the spore. Phylogenetically both species cluster with sequenced members of their respective genera. Plasmodia of E. adlardi n. sp. were encountered in 72.2% of gobies examined, and S. kenti n. sp. in 25.6%. Overall, 6.7% of animals were uninfected, and only 4.4% of the 90 fish examined were infected with both species. The observed co-occurrence was lower than expected by chance, strongly suggestive of an interaction between these species.

Apophallus microsoma N. SP. from chicks infected with metacercariae from coho salmon (Oncorhynchus kisutch) and review of the taxonomy and pathology of the genus Apophallus (Heterophyidae).

Metacercariae of an unidentified species of Apophallus Lühe, 1909 are associated with overwinter mortality in coho salmon, Oncorhynchus kisutch (Walbaum, 1792), in the West Fork Smith River, Oregon. We infected chicks with these metacercariae in order to identify the species. The average size of adult worms was 197 × 57 µm, which was 2 to 11 times smaller than other described Apophallus species. Eggs were also smaller, but larger in proportion to body size, than in other species of Apophallus. Based on these morphological differences, we describe Apophallus microsoma n. sp. In addition, sequences from the cytochrome c oxidase 1 gene from Apophallus sp. cercariae collected in the study area, which are likely conspecific with experimentally cultivated A. microsoma, differ by >12% from those we obtained from Apophallus donicus ( Skrjabin and Lindtrop, 1919 ) and from Apophallus brevis Ransom, 1920 . The taxonomy and pathology of Apophallus species is reviewed.

Seasonal and yearly population dynamics of two exotic helminths, Camallanus coti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O'ahu, Hawaii.

Exotic poeciliid fishes introduced into Hawaiian freshwaters are responsible for the introduction of several exotic parasites, of which the most important are Camallanus cotti and Bothriocephalus acheilognathi in terms of potential disease threat to native stream fishes. This roundworm and tapeworm are the most prevalent and abundant freshwater fish helminths in Hawaiian streams. This study examined the seasonal and yearly population structure of C. cotti and B. acheilognathi to determine if the tropical Hawaiian environment characterized by low climatic variability permits continuous opportunities for parasite transmission regardless of time of year. Camallanus cotti displayed seasonal differences in prevalence and mean abundance, whereas B. acheilognathi did not. Camallanus cotti prevalence and mean abundance were higher in the Hawaiian summer (47.7%, 0.79) than in winter (25.8%, 0.36). A seasonal relationship of C. cotti levels is likely explained by extensive rains associated with the Hawaiian winter season, which may act to decrease parasite transmission by flushing infected poeciliid hosts, intermediate copepod hosts, and possibly free-living infective worm stages downstream. Bothriocephalus acheilognathi displayed low prevalence and mean abundance in both summer (4.0%, 0.06) and winter (6.5%, 0.07), and it may be difficult to detect seasonal changes due to these low levels. Camallanus cotti prevalence and mean abundance remained relatively constant from the summer of 1995 to the summer of 1999, indicating that levels of this roundworm are stable in Waianu Stream. Whereas B. acheilognathi prevalence and mean abundance were low during the summer of 1995 and the summer of 1997, a dramatic peak in prevalence and mean abundance was observed in the summer of 1998 (41.2%, 1.06), with levels decreasing sharply in the summer of 1999 (4.4%, 0.07). It appears that B. acheilognathi also is present in stable populations at low levels, even though levels rose sharply during a single year.

Host specificity and population structure of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O'ahu, Hawai'i.

Introduction of exotic fishes into Hawai'ian streams has resulted in the simultaneous introduction of exotic parasites. Camallanus corti (Nematoda) and Bothricephalus acheilognathi (Cestoda) are the most prevalent and abundant fish helminths in Hawai'ian streams. The population structure and host specificity of C. cotti and B. acheilognathi in exotic poeciliids were examined during May and June 1995 in Waianu Stream, O'ahu, Hawai'i. Prevalence and mean abundance of C. cotti were significantly different among Poecilia reticulata (65.2%, 1.05), Poecilia mexicana (49.0%, 0.87), and Xiphophorus helleri (32.3%, 0.44). Prevalence of B. acheilognathi was significantly higher in P. mexicana (6.1%) than in P. reticulata (2.1%) and X. helleri (1.6%). However, tapeworm differences in mean abundance were not significant among P. mexicana (0.08), P. reticulata (0.04), or X. helleri (0.03). Nematode and tapeworm prevalence and mean abundance were not significantly different with regard to fish sex. Camallanus cotti prevalence and mean abundance increased as P. mexicana body size increased (r2 = 0.84 and r2 = 0.72, respectively), whereas B. acheilognathi displayed no significant trend with respect to poeciliid body size.

Seasonal dynamics of the helminths of bluegill (Lepomis macrochirus) in a subtropical region.

Seasonal prevalence and abundance of the helminths of bluegill sunfish in a Louisiana oligohaline bayou were measured by a survey and a field "live-box" experiment. The survey took place from the spring of 1997 to the summer of 1998 and examined fish that were <7 cm. Three trematode species, Phagicola nana (Heterophyidae), Ascocotyle tenuicollis (Heterophyidae), and Posthodiplostomum minimum (Diplostomatidae), and 2 nematode species, Camallanus oxycephalus (Camallanidae) and Spinitectus carolini (Cystidicolidae), were examined. Camallanus oxycephalus was the only helminth that showed a distinct seasonal pattern. Abundance and prevalence peaked in summer, which was likely driven by concerted reproductive cycles of females. The survey data indicated that the other helminths fluctuated over time but did not seem to follow a distinct seasonal pattern. The fluctuations could be attributed to the variable nature of the habitat or to the stochastic events that influence transmission dynamics, particularly isolated events such as tropical storms, which cause dramatic changes in salinity. The live-box experiment successfully measured recruitment of A. tenauicollis and suggested a seasonal component of the distribution of this species, which was possibly caused by temperature-dependent emergence of cercariae from the snail intermediate host.