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Gonochorism and Degrees of Monogamy in Schistosomes - Essay Example

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In this paper "Gonochorism and Degrees of Monogamy in Schistosomes" an effort has been made to shed light on the various theories on the evolution of gonochorism and how this unique feature of the parasite affects their mating behaviour…
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Gonochorism and Degrees of Monogamy in Schistosomes
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The mating game- Gonochorism and degrees of monogamy in schistosomes Schistosomiasis, or bilharzia is a parasitic disease caused by trematodes of the genus schistosoma and is considered by the world health organization as the second most important disease only to malaria, infecting hundreds of millions globally. Schistosomes themselves are as intriguing as the disease itself, exhibiting attributes that are unique to the genus (Combes 1991). One such attributes is the distinct sexual dimorphism as opposed to hermaphrodism which is the rule in other species of trematodes. This feature among schistosomes is very interesting as it is usually considered that dioecy is disadvantageous to parasites. This article essays the implication of this unique physiological characteristic and its consequences on schistosome life history particularly their faithfulness while choosing a mate. Adult schistosoma lives in the mammalian blood but their life cycle requires a phase of asexual reproduction within a secondary host. The life history of the parasite begins when adult female deposit eggs in the veins surrounding intestine or bladder. The mammal then continues the life cycle by transmitting those eggs through urine or feces. Once in water, the eggs hatch into marcidia, which must find an appropriate snail host. Once inside the snail each marcidium produce several hundreds of carcariea which when released in water seeks the skin of suitable mammals to burrow into. There are many different species of schistosomes of which Schistosoma haematobium, S. mansoni, and S. japonicum clinically important parasites that infect humans. Schistosoma haematobium , commonly called urinary schistosomiasis, dwells in the vesical veins surrounding the urinary tract and therefore mammal host usually excretes its eggs in urine. It is found throughout most of Africa and in parts of Western Asia. Two species, S. mansoni and S. japonicum cause intestinal schistosomiasis. S. mansoni usually occupies the mesenteric veins around the large intestine,while S. japonicum usually occupies the mesenteric veins around the small intestine. The mammalian host excretes the eggs in feces and continues the life cycle. Figure 1: Life cycle of Schistosoma (Machen, Rogers n.d.) Gonochorism is a reproductive strategy that describes a sexually reproducing species in which there are two distinct sexes. It is a very unique characteristic exhibited by schistosomes and thus this unusual physiological state managed to raise considerable amount of curiosity amongst parasitologists over the past two decades. Loker (2006) in his most recent study has put forward a hypothesis to address the foundattion of schistosome gonochorism. He says that first, schistosomes were derived from hermaphroditic ancestors; second, the potential for gonochorism appeared in the spirorchiids, most notably with Griphobilharzia; and third, 'true gonochorism' appeared when schistosomes invaded their endothermic hosts (birds and mammals). The evolution of separate genders was supposedly beneficial in providing optimal genetic diversity against the sophisticated immune system of warm-blooded vertebrate hosts. Loker (2006) also suggest that the segregation of two genders was determined by the specialization of each gender for a limited set of 'domestic task' and this was further backed by the gender associated gene expression profiling study by (Hoffman et al. 2002). It was concluded that males primarily looks after the transportation while females concentrate on egg production. In such an interaction schistosomes, once paired, the male and the female worms remains in this state for a long time and the mating is assumed to be monogamous (Reed 1990). In most of the Schistosomes, pairing is essential for complete female growth and reproductive morphogenesis (Popiel 1986). Figure 2: A typical schistosoma pairing (Beltran 2008, p.2) Kunz (2001) demonstrated that virgin females (one sex females) are considerably smaller than paired females and it is already established that egg laying female schistosomes separated from their male partners and surgically implated in nave animal stops laying eggs and starts regressing physically and reproductively to the immature state (Clough 1981; Popiel 1981& Popiel 1984). These studies taken together reiterate the important role of male schistosomes. Thus an intimate and permanent physical contact is necessary for successful reproduction. There are different factors that have been proposed to explain the sexual maturity of schistosomes including physical/tactile contact (Popiel et al. 1984, Armstrong 1965 & Michael, 1969.), nutrition (LoVerde, 2004; Gupta 1987) and chemical stimuli (Shaw 1977; Silveira et al. 1986 & Haseeb 1998). The role of genetic stimulus was put forward by Weisberg et al. (2007) by comparing mature and immature worms identified several new maturation associated transcripts. He found that of the 256 differentially expressed transcripts 55% were highly expressed in paired females compared to unpaired ones and about 56.6% of total 53 differentially expressed genes were found to be upregulated in adult males. The role of female parasite in morphological development on male worms are however subtle and has received less attention. Nevertheless Seigel (1988 & 1989) in two independent study showed that female schistosomes influences biochemical and molecular chances in the male metabolism. For instance glutathione level in single sex males are much higher than the paired ones. In other examples paired schistosomes expresses a 79 kDa protein in its gynecophoral canal and that this protein is resticted only at the surface of unpaired worms (Bostic 1996). Dioecy of schistosomes has created a great opportunity for interactions between male and female. Armstrong (1965) for the first time pointed out the mating behavior nd development of schistosomes in mouse. He showed that pairing occurred out of regard between species and the pairing attraction was thigmotactic rather than chemotactic. However the role of chemo-attractant in the mating process was later confirmed in vitro many investigators (Eveland et al.1982a, Imperia 1980, Evaland & Fried 1987). Detailed study of mating behavior in mixed population of schistosomes has opened new avenues. In two different study Tchuem Tchuente (1993) and Fried (1990) has shown in a S. intercalatum and S.masoni model that there exists a specific mate preference system leading to mating competition and the possibility of change of mate. Despite S. intercalatum and S.masoni belonging to different evolutionary lineages, immediate heterologous pairing was observed in the absence of choice of mate (Tchuem Tchuente 1993). However in simultaneous infection with choice of mate clearly revealed the existence of specific mate preference system and that S.masoni showed greater specific preference than S. intercalatum. These data taken together showed that intra masoni attraction/recognition is much stronger than intra intercalatum and the differences between inter and intraspecific chemo attractant (Fried 1990). Tchuem Tchuente (1995) also showed that S. masoni males are better at pairing than S. intercalatum strains and given the opportunity they will change partner to pair with heterologous females. In fact it was observed that in the absence of S. masoni female worms the males were able to pull away female worms from a pre-established S. intercalatum infection. This indicates the strong competitiveness of male S. mosoni and raises question about the site of such interchange. Monogamy is a mating behavior where the male engages in mating relationship with a single female over a period of time. Reichard and Boesch (2003) showed that monogamy could be observed at different levels like social and genetic. In a social monogamy organisms are seen to remain in pair without implying sexual exclusivity whereas in a genetic monogamy the offspring is exclusive result of two distinct parents (Hughes 1998; Danchin et al. 2005). Genetic monogamy is extremely rare and cases showing offspring resulting from mate changes have been demonstrated in birds (Birkhead and Moller 1995), reptiles (Bull 2000) and mammals (Goossens et al. 1998). The classical view of worm couple indicates that schistosomes are socially monogamous. However whether genetically monogamy exists among them needs further consideration. Phylogenetic analysis of mating system indicates the origin of the monogamy in schistosomes. Figure 3: Map of the mating system on schistosome phylogeny (Beltran, Boissier 2008) The above figure shows that the mating system is independent of the vertebrate host group (birds or mammals) and that monogamy should be ancestral state. Indeed, the more basal gonochoric schistosome, Griphobilharzia, is monogamous, and even if we do not know enough about the mating behaviour of schistosomes to conclude that some branches of the schistosome tree were monogamous and some were not, species (except A. variglandis) of the ancestral AO clade (Austrobilharzia and Ornithobilharzia genera) and species of the BSO clade (Schistosoma, Orienthobilharzia and Bivitellobilharzia genera) seem to be monogamous, whereas species of the more recent clades, the SH clade (Schistosomatium and Heterobilharzia genera) and the BTGD clade (Bilharziella, Trichobilharzia, Gigantobilharzia and Dendritobilharzia genera), seem to be polygamous or polygynandrous (Beltran, Boissier 2008). The monogamous mating system of schistosomes seems to be an intermediate state between hermaphroditism and polygamy or polygynandry. Loker (2006) hypothesized that the ancestral origin of monogamy could corroborate the hypotheses on the origin of gonochorism. Gonochorism would appear when schistosomes have invaded their endothermic hosts (birds and mammals) because of the necessity to exploit a peculiar habitat, which has advanced immune sysytem: the hepatic portal system (Loker 2006). The necessity to both resist against portal blood flow and to move into the tiniest venules to release eggs results in a division of labour between a muscular male and a thin female (Despres 1995) The separation of the genders would obviously bring on sexual interdependence (spermatozoide and ovocyte) but would also encourage functional interdependence. The monogamous mating system would compensate for this male-female functional interdependence (Beltran, Boissier 2008). There are three hypotheses that classically explain the evolution of monogamous behavior in free-living animals. They are dispersal of females; paternal care and the reverse polygyny threshold hypothesis (Reichard 2003). Female dispersion in schistosome from liver to mesenteric veins is the key feature. Some schistosome species corroborate the hypothesis (H. americana) while others do not like S. mansoni (Armstrong 1965). Female dispersion study has been conducted only on H. americana, S. mansoni and S. douthitti, which means generalizing the hypothsis is difficult. Paternal care is often considered as the origin of monogamy in schistosomes (Read, Nee 1990) (Morand and Muller-Graf 2000). By helping female to reach egg-laying site and attain sexual maturity males increases the survival rate and thus takes care of its progeny. However this does not conclusively proves monogamy (Smith et al. 1995) but could only be a consequence of gonochorism (Locker, Brant 2006). Reverse polygyny threshold hypothesis could be another factor for encouraging monogamy. Thus in the absence of variation in quality of males a female would restrict herself to a single male rather than involving herself in a polygynous relationship. In terms of resources, if the egg laying venules are considered as territories then an over influx of paired egg laying schistosomules might ruin the site by formation of granuloma around the aggregates of eggs. Thus fact that resources are limited and evenly distributed in space agrees with the reverse polygyny threshholh hypothesis and could therefore explain monogamy in some schistosome species. (Beltran, Boissier 2008). Pica-Mattoccia, L. et al. (2000) has shown that S. mansoni practice mate changing in a mixed population infection at an estimated rate of 28% when mates were resistant to a particular drug and at 8% when the mates where sensitive to a drug. However the author also mentions that the use of pharmacological markers induces a bias in the rate of change in mates. Therefore Beltran and Boissier (2008) acknowledge the importance of neutral genetic markers like microsatellites in determining the rate of mate changes without any bias. It is essential to know which gender amongst schistosomes initiates mate change. Classical theory of sexual selection (Triver's 1972) points out female as the choosy gender. In schistosomes, experimental evidence shows (Pica-Mattoccia et al. 2002) that newcomer males in an established infection were able to displace the male from a pre-existing worm couple. This observation was found in previous intrerspecific experiments works of Tchuem-Tchuente et al (1993 1995 & 1996) and Southgate et al (1998). Thus a completely new trend in mate change is found in Schistosome. However it the role of female schistosome in mate selection should not be disregarded and for to substantiate the role of female worms in mate selection should be determined invitro (Beltran and Boissier 2008). In their study Beltran, Cezilly & Boissier (2008) showed that female preference for dissimilar males results in more heterozygous offsprings. Correlation study (Roberts, Hale & Petrie 2006) shows that both heterozygosity and genetic similarity can trigger female choice of mate and this two should be simultaneously studied in analyses of mate choice (Mays, Hill 2004)(Robert, Gosling 2003)(Bishop, O'Ryan & Jarvis 2007). "Divorce" is another interesting phenomenon that has been seen in Schistosoma. Studies conducted by Pica-Mattoccia et al. (2000) have demonstrated this fact in S. masoni. According to good-genes-as heterzygosity (Brown 1997 and Weatherhead et al 1999) females should always choose partener with higher level of heterozygosity however in their study Beltran, Cezilly and Boissier (2008) found out that genetic dissimilarity but not male heterozygosity has positive effect on parasite divorce. Schistosomula are classically known to be socially monogamous. Offspring genotyping can only answer whether these worms are genetically monogamous or not. In a short communication Beltran and Boissier (2009) sheds light on this issue. Here DNA analysis confirms rapid offspring production resulting from mate change despite the potential ability for female schistosomes to store sperm in their receptaculum seminis (Erasmus 1973; Neves et al. 2005). Figure 4: Rate of offspring resulting from mate change in S. mansoni during course of parasitic infection. (Beltran , Boissier 2009) The above figure depicts the rate of offspring resulting from mate change in S. mansoni during the course of the parasite infection. The numbers in each histogram shows the number of offspring genotyped. Beltran and Boissier (2009) points out that offspring from the second mate resulted 9 weeks after the first infection and there was an over all 21% offspring produced from mate change. This study is one of its kinds because it shows for the first time that rapid offspring production can take place in monogamous invertebrate in absence of choice of mate. This study strongly points out that schistosomes are socially but not genetically monogamous. Schistosoma are considered to be the best suited model for the study of monogamy as they are devoid of complexities like learning, hierarchy etc. However not enough is known about mating behavior of these parasite. Here, in this essay, effort has been made to shed light on the various theories on evolution of gonochorism and how this unique feature of the parasite affects is mating behavior. Several experimental data has been put forward that indicates the presence of different modes in which these parasites attracts mates and also the existence of competition while sexual pairing. Finally the most intriguing and most fascinating aspect of schistosome mating system: monogamy has been discussed in details. However questions like where mating interaction occurs and who initiates those are not well understood. Therefore more knowledge is required to address several of these unexplained or poorly understood behaviors in schistosomes. A complete understanding of these issues might open up new avenues in drug discovery and eventually might help in controlling the disease. Reference: Armstrong, J,C 1965 'Mating behavior and development of schistosomes in the mouse', J Parasitol, vol. 51, pp.605-616. 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