Abstract

An understanding of the mechanisms influencing prenatal characteristics is fundamental to comprehend the role of ecological and evolutionary processes behind survival and reproductive success in animals. Although the negative influence of parasites on host fitness is undisputable, we know very little about how parasitic infection in reproductive females might influence prenatal factors such as fetal development and sex allocation. Using an archival collection of Dall’s sheep (Ovis dalli dalli), a capital breeder that depends on its body reserves to overcome the arctic winter, we investigated the direct and indirect impacts of the parasite community on fetal development and sex allocation. Using partial least squares modelling, we observed a negative effect of parasite community on fetal development, driven primarily by the nematode Marshallagia marshalli. Principal component analysis demonstrated that mothers with low parasite burden and in good body condition were more likely to have female versus male fetuses. This association was primarily driven by the indirect effect of M. marshalli on ewe body condition. Refining our knowledge of the direct and indirect impact that parasite communities can have on reproduction in mammals is critical for understanding the effects of infectious diseases on wildlife populations. This can be particularly relevant for species living in ecosystems sensitive to the effects of global climate change.

Highlights

  • An understanding of the mechanisms influencing prenatal characteristics is fundamental to comprehend the role of ecological and evolutionary processes behind survival and reproductive success in animals

  • Parasites can affect fetus development through several pathways including (i) a direct effect of parasite virulence on fetal development or survival causing pregnancy failure, as seen with bacteria such as Brucella abortus and protozoa such as Neospora caninum[21,22], (ii) an indirect effect of the energetic cost of parasitic infection on the mother, resulting in decreased nutrition to the fetus and a developmental d­ elay[23,24], and (iii) an indirect effect of parasites interrupting or delaying pregnancy due to a negative effect on host condition resulting in delayed ovulation and conception, which can translate to smaller fetus ­size[25]

  • We found that gastrointestinal helminths, and M. marshalli, were both directly and indirectly associated with lighter and smaller fetuses in Dall’s sheep

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Summary

Introduction

An understanding of the mechanisms influencing prenatal characteristics is fundamental to comprehend the role of ecological and evolutionary processes behind survival and reproductive success in animals. Principal component analysis demonstrated that mothers with low parasite burden and in good body condition were more likely to have female versus male fetuses This association was primarily driven by the indirect effect of M. marshalli on ewe body condition. Refining our knowledge of the direct and indirect impact that parasite communities can have on reproduction in mammals is critical for understanding the effects of infectious diseases on wildlife populations. Mating systems, mothers in good condition will produce more sons than daughters because they can afford to provide the needed maternal care to produce a high-quality son This strategy yields the greatest fitness return in species where variance in reproductive success is strongly correlated with body size in males but not in females. The role of mother’s parasitic infection on sex allocation has not been documented in wild mammals, studies investigating the influence of protozoan parasite, Toxoplasma gondii, in sex allocation of people and mice have demonstrated an important link between this parasite and sex a­ djustments[35,36,37]

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