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Density-Dependent Sex Ratio and Sex-Specific Preference for Host Szentiványi et al. Parasites & Vectors (2017) 10:405 DOI 10.1186/s13071-017-2340-0 RESEARCH Open Access Density-dependent sex ratio and sex- specific preference for host traits in parasitic bat flies Tamara Szentiványi1,2,3*†, Orsolya Vincze4,5† and Péter Estók6 Abstract Background: Deviation of sex ratios from unity in wild animal populations has recently been demonstrated to be far more prevalent than previously thought. Ectoparasites are prominent examples of this bias, given that their sex ratios vary from strongly female- to strongly male-biased both among hosts and at the metapopulation level. To date our knowledge is very limited on how and why these biased sex ratios develop. It was suggested that sex ratio and sex- specific aggregation of ectoparasites might be shaped by the ecology, behaviour and physiology of both hosts and their parasites. Here we investigate a highly specialised, hematophagous bat fly species with strong potential to move between hosts, arguably limited inbreeding effects, off-host developmental stages and extended parental care. Results: We collected a total of 796 Nycteribia kolenatii bat flies from 147 individual bats using fumigation and subsequently determined their sex. We report a balanced sex ratio at the metapopulation level and a highly variable sex ratio among infrapopulations ranging from 100% male to 100% female. We show that infrapopulation sex ratio is not random and is highly correlated with infrapopulation size. Sex ratio is highly male biased in small and highly female biased in large infrapopulations. We show that this pattern is most probably the result of sex-specific preference in bat flies for host traits, most likely combined with a higher mobility of males. We demonstrate that female bat flies exert a strong preference for high host body condition and female hosts, while the distribution of males is more even. Conclusions: Our results suggest that locally biased sex ratios can develop due to sex-specific habitat preference of parasites. Moreover, it is apparent that the sex of both hosts and parasites need to be accounted for when a better understanding of host-parasite systems is targeted. Keywords: Bat fly, Chiroptera, Density-dependence, Parasite intensity, Sex ratio Background within-species variance can be attributed to different Host-parasite interactions are of key importance in evo- life-history strategies of male and female hosts [2, 3]. On lutionary biology, defining coevolutionary arms races, the other hand, parasites target the most efficient ex- demography and fitness of both hosts and parasites [1]. ploitation of their hosts and maximisation of their own On the one hand, the reproductive output of hosts reproductive output. Nonetheless, sexual differences are largely depends on their ability to avoid or mitigate para- often observed in parasite species including dimorphism site burden that require various adaptations at the level in size, mobility, behaviour, competitive ability, or even of behaviour and physiology. These adaptations often genetic structure [4–6], likely to result in sex-specific differ between host individuals and large part of this fitness maximisation strategies, similarly to their hosts. Accounting for sex differences in hosts and their para- sites is therefore of equal importance when a better * Correspondence: [email protected] †Equal contributors understanding of host-parasite systems is targeted. 1Department of Evolutionary Zoology and Human Biology, University of Some of the most intriguing current conundrums of Debrecen, Egyetem tér 1, H-4032, Debrecen H-4032, Hungary parasitology appear to be closely linked to parasite sex. 2Department of Ecology and Evolution, University of Lausanne, Biophore, CH-1015 Lausanne, Switzerland For example, biased sex ratios are common in ectopara- Full list of author information is available at the end of the article sites and despite strong scientific attention, driving © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Szentiványi et al. Parasites & Vectors (2017) 10:405 Page 2 of 9 causes of sex ratio distortions remain controversial in isolated populations, especially with limited male disper- this group [5, 7, 8]. The most common sex ratio in ecto- sal and considerable sibmating, parents and sons com- parasites is female-biased, but equal and strongly male- pete for mating opportunities. In such populations biased sex ratios are also commonly encountered both fitness returns of female offspring is higher than of on a species level and within species, among different males, therefore adaptive adjustment in offspring sex host individuals [5, 7]. It remains to be explored why sex ratio occurs. The degree of inbreeding in bat flies is little ratios of parasite populations vary so widely and what known [5], but appears to be considerably low since adaptive significance do sex ratio fluctuations have [6]. chances of host switching is high. It is therefore unlikely Bats represent widely used model organisms for para- that the LMC plays a significant role in shaping adult sitological studies and they are hosts to a high diversity sex ratios of bat flies. of parasites. Among ectoparasites, four insect orders Sex-specific longevity is another parasite trait that is have been recorded on bats, including bat flies (Diptera), likely to bias adult sex ratios in ectoparasitic arthropods, fleas (Siphonaptera), true bugs (Hemiptera) and earwigs toward an excess of the sex with the longer lifespan [7]. (Dermaptera) [1]. Bat flies are present with two families, In nycteribiid bat flies sex-specific longevity has been Nycteribiidae and Streblidae, with 16 species of nycteri- documented before; average lifespan of males was biids and only one streblid species recorded in Europe 136 days, while that of females reached 195 days in B. to date [9]. Nycteribiids are obligate, wingless, highly hipsida [12]. Similarly, female-biased longevity was specialised blood-feeding ectoparasites of bats. They observed in a few closely related fly species [5]. None- reproduce by adenotrophic viviparity; females produce a theless, it is little known how general this sex-specific single offspring at a time, the egg and then the larva longevity is among different bat fly species and how develops, feeds, moults within the uterus and consumes significant its role is in shaping adult sex ratios. Other the secretion of special “milk glands”. Pregnant females important factors, probably not independent of longev- leave their hosts to larviposit the third-instar larvae on ity, are sex-specific body size, mobility and detectability. the walls of the host’s roosting sites. The deposited larva Such differences might result in higher probability of a pupates immediately and adult flies usually emerge certain sex to be found or picked by the host or within 3 to 4 weeks following pupation [1]. This highly collected by human observers. These can result in sex- specialised host-parasite system provides an exceptional specific grooming or sampling bias, respectively. opportunity to study host-parasite interactions due to its Similarly, sex-specific diurnal behaviour, especially rare properties. Bats roost communally, with high fre- concerning off-host behaviours, such as larviposition quency of prolonged physical contact among dozens to might contribute to sampling bias and erroneous sex hundreds of individuals, providing ectoparasites with the ratio estimates [5, 8]. possibility of free movement between hosts and to Besides fluctuation in their sex ratios bat flies exhibit perform active choice of hosts. Moreover, off-host devel- considerable variance in their aggregations both at the opmental stages and larviposition, the relatively long, intra- [14] and interspecific levels [15] even when hosts off-host metamorphosis of the larvae, as well as the roost in close physical contact. Most host individuals sequential roost site utilisation ensures genetic mixing of harbour no or only a small number of parasites and only a parasites among hosts. These characters largely reduce few bear with higher parasite intensities (e.g. [16]). Infest- inbreeding, a factor that has been suggested to deeply ation rates of hosts appear to be influenced by a wide influence demography and population dynamics of most range of behavioural, physiological and ecological traits of parasite species. both hosts and their parasites. Among host traits, sex ap- Several hypotheses have been proposed to explain sex pears to play a particularly important role in this respect, ratio variation in arthropod ectoparasites. These include partly due to sex-specific parasite exposure. In bats for in- biased prepartum sex ratio, local mate competition, sex stance females tend to roost in colonies, while males usu- differences in longevity, selective grooming or sampling ally roost solitarily or in small aggregations [17–20]. This bias [1, 5, 7, 10, 11]. Skewed sex ratios of bat flies at difference is often mentioned as a key factor
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