Castration of Female Ninespine Stickleback by the Pseudophyllidean Cestode Schistocephalus pungitii: Evolutionary Significance and Underlying Mechanism

Abstract

Parasitic castration may result from manipulation of host energy allocation away from reproduction, which should result in castration of lightly infected hosts as well as heavily infected ones. Castration also may result from nutrient theft alone, which incidentally influences host energy allocation to reproduction and should cause reproduction to end in heavily infected hosts. Although the pseudophyllidean cestode Schistocephalus pungitii is a castrator of ninespine stickleback fish (Pungitius pungitius), the cause and significance of castration remain unknown. We used predictions about reproductive capacity in lightly and heavily infected hosts and host size (age) at which castration occurs to address these questions. In Airolo Lake, Alaska, we found that inhibition of reproduction in ninespine stickleback occurs in small fish before the size (age) of sexual maturity and is not instantaneous. Castration was observed in lightly and heavily infected adult-size hosts. Infected fish do not reach the same size as uninfected fish, possibly because of growth inhibition or selective predation. Castration in infected adult-size female ninespine stickleback appears to be the result of adaptive manipulation of host energy allocation by the parasite, but it could result from an energy budget readily influenced by parasitism.

Fecundity compensation in the three-spined stickleback Gasterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus

“…As the nutrient theft takes its toll on the energy levels of the host, measures of reproductive performance should decline. As a result, clutch mass, egg number, and ovum mass should decrease as the severity of infection, measured by the parasite : host biomass ratio, increases until reproduction ceases or the host dies before reproduction ends in very heavily infected hosts late in an infection (Javadian & MacDonald, 1974; Hurd, 2001; Hall et al ., 2007; Heins & Baker, 2010).…”

“…In G. aculeatus , with infections typically occurring before sexual maturity (Heins & Baker, 2011; Heins et al ., 2011), parasitic manipulation should cause sterility among juvenile fish before reaching the size (age) at which reproduction begins. A small percentage of lightly infected fish may reproduce because sterilization may not be instantaneous (Heins & Baker, 2010).…”

Distinct Lineages of Schistocephalus Parasites in Threespine and Ninespine Stickleback Hosts Revealed by DNA Sequence Analysis

“…Oceanic threespine stickleback have repeatedly given rise to derived freshwater populations that have evolved along many phenotypic axes [34], [35], including the ability to cope with a large number of parasites that differ according to the habitat in which they are found [36]. The ninespine stickleback ( Pungitius pungitius ) is well supported as the sister lineage to threespine stickleback, and is also being developed into a model for evolutionary and ecological studies [37]–[42]. Ninespine stickleback also has a widespread, circumarctic distribution that frequently overlaps with threespine stickleback, and the two species can co-occur in the same lakes and rivers [21], [43].…”

Evolutionary significance of fecundity reduction in threespine stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus

“…Manipulation of host energy allocation and simple nutrient theft are different life‐history tactics, which should produce demonstrably different effects on host reproductive function, revealing the strategy of the parasite (Hall et al ., 2007; Heins & Baker, 2010). Castration arising from parasitic manipulation of host energy allocation should occur early in infections (Hall et al ., 2007) and be observed among both lightly‐ and heavily‐infected hosts (Hacker & Kilama, 1974; Renshaw & Hurd, 1994; Hogg & Hurd, 1995; Hurd, 2001).…”