The Seychelles Warbler and Other Congeners

Conserv Genet (2016) 17:661–674 DOI 10.1007/s10592-016-0813-x RESEARCH ARTICLE Avian b-defensin variation in bottlenecked populations: the Seychelles warbler and other congeners 1 2 3 1,4 Danielle Gilroy • Cock van Oosterhout • Jan Komdeur • David S. Richardson Received: 24 February 2015 / Accepted: 18 January 2016 / Published online: 1 February 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract b-defensins are important components of the AvBD11. Variation in the Seychelles warbler was signifi- vertebrate innate immune system responsible for encoding cantly lower than in the mainland migratory congeneric a variety of anti-microbial peptides. Pathogen-mediated species investigated, but it similar to that found in other selection is thought to act on immune genes and potentially bottlenecked species. In addition, screening AvBD7 in 15 maintain allelic variation in the face of genetic drift. The museum specimens of Seychelles warblers sampled prior to Seychelles warbler, Acrocephalus sechellensis, is an the bottleneck (1877–1905) revealed that this locus pos- endemic passerine that underwent a recent bottleneck in its sessed two alleles previously, compared to the single allele last remaining population, resulting in a considerable in the contemporary population. Overall, the results show reduction in genome-wide variation. We genotyped avian that little AvBD variation remains in the Seychelles war- b-defensin (AvBD) genes in contemporary (2000–2008) bler, probably as a result of having low AvBD diversity and museum samples (1876–1940) of the Seychelles war- historically rather than the loss of variation due to drift bler to investigate whether immunogenetic variation was associated with past demographic history. Given the lim- lost through this bottleneck, and examined AvBD variation ited pathogen fauna, this lack of variation at the AvBD loci across four other Acrocephalus species with varying may currently not pose a problem for this isolate popula- demographic histories. No variation was detected at four of tion of Seychelles warblers, but it may be detrimental to the the six AvBD loci screened in the post-bottleneck popu- species’ long-term survival if new pathogens reach the lation of Seychelles warbler, but two silent nucleotide population in the future. polymorphisms were identified at AvBD8 and one potentially functional amino-acid variation was observed at Keywords Seychelles warbler Á Avian b-defensins Á Bottleneck Á Demographic processes Á Genetic drift Á Selection Electronic supplementary material The online version of this article (doi:10.1007/s10592-016-0813-x) contains supplementary material, which is available to authorized users. Introduction & David S. Richardson [email protected] Drift is the predominant evolutionary force shaping genetic variation in small populations (Hedrick et al. 2001; Miller 1 School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK and Lambert 2004; Jensen et al. 2013), and its effects on genetic variation often outweigh the influence of selection 2 School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK (Miller and Lambert 2004; Alcaide 2010; Grueber et al. 2013). Nevertheless, various studies have shown that 3 Behavioural Ecology and Self-Organization, Centre for Ecological and Evolutionary Studies, University of within small natural populations, variation at specific key Groningen, 9700 CC Groningen, The Netherlands loci can be elevated above that of the genome-wide aver- 4 Nature Seychelles, P.O. BOX 1310, Mahe, Republic of age, and be maintained across bottleneck events as a result Seychelles of balancing selection (Aguilar et al. 2004; Tompkins 123 662 Conserv Genet (2016) 17:661–674 2007; van Oosterhout et al. 2006). Given that a loss of immune repertoire (Selsted and Ouellette 2005). For exam- genetic variation within a population impacts on both ple, birds have only b-defensins, of which 14 different loci inbreeding depression and adaptive potential (for review, have been identified in the domestic chicken, Gallus gallus see Garrigan and Hedrick 2003), the maintenance of domesticus (Lynn et al. 2004; Xiao et al. 2004), whereas polymorphisms at key loci will be important to a popula- mammals have both a and b-defensins (Yang et al. 2002). tions’ long-term viability (Meyers and Bull 2002; Ellegren The number of b-defensins in a species has been shown to and Sheldon 2008; Zhu et al. 2013). However, not all highly relevant to the ever-changing microbial challenges of immune genes are under balancing selection (Mukherjee the environment in which that species’ inhabits (Tu et al. et al. 2009). By performing a temporal analysis comparing 2015). It has been well-shown that different defensin alleles variation before and after a bottleneck event it is possible have different antimicrobial activities in vitro in a range of to discern the effects of balancing selection. Furthermore, vertebrate hosts (Meredith et al. 2008; Mukherjee et al. 2009; taking a candidate-gene approach and focusing on those Hellgren et al. 2010; Chow et al. 2012). These studies suggest loci most likely to be under selection in natural populations that the greater the variety of AMPs encoded, the greater the (Fitzpatrick et al. 2005), avoids inflating the possibility of ability to combat a range of bacteria. These studies therefore type 1 errors. suggest that there could be an advantage to individuals (and Genes that contribute to immune function are ideal can- populations) which are heterozygous at these loci. didates with which to assess the roles of drift and selection in Birds provide excellent systems in which to study the maintaining functional diversity within natural populations causes and consequences of innate immune gene variation (for review, see Acevedo-Whitehouse and Cunningham under natural conditions. Functional variation at defensin 2006). Many such studies have focused on the highly poly- genes has been shown to exist within and among species morphic genes of the major histocompatibility complex (for review, see van Dijk et al. 2008) and locus-specific (MHC), which play a central role in the acquired immune protocols have been developed to screen for avian b-de- system (Doherty and Zinkernagel 1975; Klein 1986; Piert- fensins (AvBDs) in passerines (Hellgren and Sheldon ney and Oliver 2006). However, there are complex inter- 2011). Importantly, variation within these loci has been acting evolutionary forces acting upon the MHC, including shown to influence anti-microbial properties in vitro the effects of epistasis and selection against the so-called (Hellgren and Ekblom 2010; Hellgren et al. 2010). Specific ‘sheltered load’ (van Oosterhout 2009). Additionally, fre- defensin alleles have also been shown in vitro to be asso- quent gene duplication (Eimes et al. 2011) and recombina- ciated with avian pathogens (Higgs et al. 2007; Ma et al. tion-like processes i.e., gene conversion (Ohta 1995; Spurgin 2012; Ramasamy et al. 2012), although whether individual et al. 2011) confound the interpretation of the population heterozygosity is advantageous has yet to be shown. genetic mechanisms maintaining variation at these genes. In The Seychelles warbler, Acrocephalus sechellensis,is contrast, studies of variation within natural populations in an ideal species in which to study the influence of different genes that play a role in the innate immune system are rel- evolutionary forces on AvBD genes. As a result of atively scarce (Sutton et al. 2011), despite the fact that these anthropogenic factors- this population experienced a bot- genes are often simpler in form and function than the MHC tleneck during the last century when it was on the verge of (for review, see Kaiser 2007). Variation in such genes may be extinction with ca 26 individuals remaining on a single crucial, given that the innate immune response is the first line island (Collar and Stuart 1985). As a result, considerable of defence against pathogens. Moreover, a number of innate variation has been lost across the warblers genome (Spur- immune gene families, including the toll-like receptors gin et al. 2014), although diversity appears to have been (TLRs) and cytokines, have been shown to be targets of maintained at MHC class I loci (Richardson and Wester- balancing selection (for examples, see Schlenke and Begun dahl 2003; Hansson and Richardson 2005) due to a com- 2003; Ferrer-admetlla et al. 2008; Mukherjee et al. 2009). bination of natural and sexual selection (Richardson et al. Anti-microbial peptides (AMPs) are effector molecules 2005; Brouwer et al. 2010). Given these patterns, we involved in the innate immune system. AMPs directly kill hypothesise that genetic variation could also have been invading pathogens via the disruption of membranes through maintained at other immune loci. If we can identify loci at cationic attack mechanisms (Hancock and Sahl 2006). All which variation has been maintained then we can carry out defensin molecules have six cysteine residues but are sorted association analysis between this immunogenetic variation into three classes based on their physical structure (Yang and individual fitness parameters using data collected over et al. 2002). Both a-defensins and b-defensins form beta- the last two decades. sheet dimers but they have different lengths and pairing of Here, we screened six AvBD loci in the contemporary cysteine linkages, whereas c-defensins have a cyclic

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