Parasite infestation influences life history but not boldness behavior in placental live-bearing fish

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POPULATION ECOLOGY – ORIGINAL RESEARCH

Parasite infestation influences life history but not boldness behavior in placental live‑bearing fish Andres Hagmayer1   · Andrew I. Furness2,3   · Bart J. A. Pollux1  Received: 3 June 2020 / Accepted: 24 October 2020 / Published online: 3 November 2020 © The Author(s) 2020

Abstract Parasites can negatively affect the reproductive success of hosts. Placental species may be particularly susceptible, because parasite-induced stress during pregnancy could potentially influence embryo development. Here, we examine the consequences of a trematode infestation (black spot disease, BSD) for fetal development and adult behavior in 19 natural populations of the placental live-bearing fish species Poeciliopsis retropinna (Poeciliidae) in Costa Rica. First, we observed substantial variation in parasite infestation among populations which correlated with a number of local environmental conditions (elevation, river width, depth, and flow velocity). Furthermore, we observed substantial variation in parasite infestation among females within populations associated with maternal age and size. We found that the infestation rate significantly influenced embryonic development, with more heavily parasitized females producing smaller and worse-conditioned offspring at birth, possibly, because a costly immune response during pregnancy limits, either directly or indirectly, nourishment to developing embryos. Finally, a behavioral experiment in the field showed that the infestation rate did not affect an individual’s boldness. Our study indicates that in placental live-bearing fish parasite infestation leads to reduced embryo provisioning during pregnancy, resulting in a smaller offspring size and quality at birth potentially with negative implications for offspring fitness. Keywords  Matrotrophy · Parasites · Placenta · Poeciliidae · Poeciliopsis retropinna

Introduction The life history of individuals describes how resources are allocated to different functions such as maintenance, somatic growth and reproduction (Roff 1992; Stearns 1992). Individuals have limited resources that must be competitively allocated to these different functions. This leads to trade-offs Communicated by Joel Trexler. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0044​2-020-04795​-6) contains supplementary material, which is available to authorized users. * Bart J. A. Pollux [email protected] 1



Experimental Zoology Group, Department of Animal Sciences, Wageningen University, 6708 WD Wageningen, The Netherlands

2



Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA

3

Department of Biological and Marine Sciences, University of Hull, Hull HU6 7RX, UK



and a limiting set of possible life-history strategies (Braendle et al. 2011). Parasites, which are ubiquitous in natural populations (Bush et al. 2001), can act on these trade-offs and induce shifts in the optimum of life-history traits (Michalakis and Hochberg 1994; Sheld