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      Patterns of ectoparasitism in North American red squirrels ( Tamiasciurus hudsonicus): Sex-biases, seasonality, age, and effects on male body condition

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          Abstract

          Within many species, males are often more heavily parasitised than females. Several hypotheses have been proposed to explain this phenomenon, including immunocompetence handicaps, sexual size dimorphism and behavioural differences. Here we set out to test the latter two hypotheses and make inferences about the former by assessing patterns of ectoparasitism across various life-history stages in a population of North American red squirrels ( Tamiasciurus hudsonicus). We also conducted an ectoparasite removal experiment to investigate the effects of ectoparasites on male body condition. We found that males were more intensely parasitized than females, but only during the mating period. There was no difference in ectoparasite intensity between male and female juveniles at birth or at emergence, suggesting that ectoparasites do not exploit male red squirrels for longer-range natal dispersal. Male red squirrels in our population were slightly heavier than females, however we did not find any evidence that this dimorphism drives male-biased ectoparasitism. Finally, we could not detect an effect of ectoparasite removal on male body mass. Our results lend support to the hypothesis that ectoparasites exploit their male hosts for transmission and that male red squirrels are important for the transmission dynamics of ectoparasites in this population; however, the mechanisms ( i.e., immunocompetence, testosterone) are not known.

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          Highlights

          • Host life-history stage and sex modulate observed patterns of ectoparasitism.

          • Red squirrels experienced highest flea intensities as young juveniles in the nest.

          • Sex-biases in ectoparasite intensity were only observable in adult hosts.

          • Ectoparasitism did not appear to affect the mass of adult male red squirrels.

          • Patterns of parasitism should be considered within the context of host life-history.

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          Most cited references83

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          Sex differences in parasite infections: patterns and processes.

          M Zuk (1996)
          Sex differences in parasite infection rates, intensities, or population patterns are common in a wide range of taxa. These differences are usually attributed to 1 of 2 causes: (1) ecological (sociological in humans); and (2) physiological, usually hormonal in origin. Examples of the first cause include differential exposure to pathogens because of sex-specific behavior or morphology. The second cause may stem from the well-documented association between testosterone and the immune system; sexually mature male vertebrates are often more susceptible to infection and carry higher parasite burdens in the field. Although many researchers favor one explanation over the other, the requisite controlled experiments to rule out confounding variables are often neglected. We suggest that sex differences in disease have evolved just as sex differences in morphology and behavior, and are the result of selection acting differently on males and females. Research has often focused on proximate mechanistic explanations for the sex difference in infection rates, but it is equally important to understand the generality of the patterns in an evolutionary context. Because males potentially gain more than females by taking risks and engaging in competition, sexual selection pressure has shaped male behavior and appearance to maximize competitive ability and attractiveness. Many of the classic male attributes such as antlers on deer are testosterone-dependent, putting males in what appears to be a cruel bind: become vulnerable to disease by developing an attractive secondary sexual ornament, or risk lowered mating success by reducing it. A variety of hypotheses have been put forward to explain why males have not circumvented this dilemma. The mating system of the host species will influence the likelihood of sex differences in parasite infection, because males in monogamous species are subject to weaker sexual selection than males in polygynous species. Whether these evolutionary generalizations apply to invertebrates, which lack testosterone, remains to be seen.
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            Bateman's principle and immunity.

            Jens Rolff (2002)
            The immunocompetence handicap hypothesis (ICHH) of Folstad and Karter has inspired a large number of studies that have tried to understand the causal basis of parasite-mediated sexual selection. Even though this hypothesis is based on the double function of testosterone, a hormone restricted to vertebrates, studies of invertebrates have tended to provide central support for specific predictions of the ICHH. I propose an alternative hypothesis that explains many of the findings without relying on testosterone or other biochemical feedback loops. This alternative is based on Bateman's principle, that males gain fitness by increasing their mating success whilst females increase fitness through longevity because their reproductive effort is much higher. Consequently, I predict that females should invest more in immunity than males. The extent of this dimorphism is determined by the mating system and the genetic correlation between males and females in immune traits. In support of my arguments, I mainly use studies on insects that share innate immunity with vertebrates and have the advantage that they are easier to study.
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              Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity.

              Maternal effects by which females provide their offspring with non-genetic factors such as hormones, nutrients and antibodies can have an important impact on offspring fitness. In vertebrates, maternal antibodies (matAb) are transferred from the mother, via the placenta, egg yolk or milk during lactation to offspring until they are 2 weeks (birds), 4-10 weeks (rodents) and 9 months (humans) old, respectively. matAb transfer can have direct effects on offspring growth rate in birds and rodents, probably by passively protecting the newborn from common pathogens before their endogenous immune system has matured. Indirect long-term effects of matAb transfer on the offspring's own immunity can be synergistic, if matAb act as antigen templates of the accumulated immunological experience of the mother and educate the newborn's immune system. However, it may also be suppressive if matAb reduce antigen presentation to the newborn resulting in antigen-specific blocking of offspring endogenous immunity. Our aim is to review the mechanisms and direct effects of matAb transfer in vertebrates with an emphasis on birds, outline a framework for research on the long-term effects of matAb on the endogenous immune system of the mature offspring and encourage ecological and evolutionary studies of matAb transfer in non-domesticated animals.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                10 June 2015
                December 2015
                10 June 2015
                : 4
                : 3
                : 301-306
                Affiliations
                [a ]Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T6E6V6, Canada
                [b ]Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta T2N4N1, Canada
                Author notes
                []Corresponding author. Current address: Millennium EMS Solutions Ltd., 6111 – 91 Street NW, Edmonton, Alberta, Canada. jesse.patterson@ 123456ucalgary.ca jpatterson@ 123456mems.ca
                Article
                S2213-2244(15)00025-5
                10.1016/j.ijppaw.2015.05.002
                4501535
                fc3d953f-d3b2-42bf-bb30-88502b0406e4
                © 2015 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 24 January 2014
                : 8 May 2015
                : 15 May 2015
                Categories
                Article

                body mass,ectoparasite,parasite removal,red squirrel,sex-biased parasitism,tamiasciurus hudsonicus,transmission dynamics

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