Deep divergence and apparent sex-biased dispersal revealed by a Y-linked marker in rainbow trout
Introduction
The comparison of intraspecific variability between the maternally-inherited mitochondrial genome and paternally-inherited Y chromosome has provided insights into sex-biased life history patterns for many organisms (Boissinot and Boursot, 1997, Eriksson et al., 2006, Pidancier et al., 2006). The mitochondrial genome has been used extensively to reconstruct phylogenies and examine post-glacial dispersal and phylogeographic patterns (Avise, 1986, Danzmann et al., 1998, Bernatchez, 2001). Use of Y haplotypes in comparable studies has been less extensive and limited to humans (e.g., Underhill and Kivisild, 2007) and other mammals (e.g., Tosi et al., 2003, Sundqvist et al., 2006). This limitation is because the X and Y chromosomes in fishes and amphibians are similar in genetic content and their Y-specific regions are relatively small and challenging to isolate (Schartl, 2004, Kondo, 2006, Smith and Voss, 2009). Although only about 10% of all fish species show morphologically apparent sex chromosomes, a high proportion appear to show a simple genetic mechanism with a single chromosome having a major influence on sex determination (Devlin and Nagahama, 2002). Thus, the isolation of additional Y-specific sequences in fishes and other non-mammalian vertebrates will likely enable the evolution of Y-specific markers to be studied in many of these animals.
The rainbow trout is an economically important sport and food fish with a native distribution on both sides of the North Pacific Ocean. The subspecies and classification of rainbow trout have been reviewed by Behnke (2002). The two most widespread subspecies are the coastal rainbow (Oncorhynchus mykiss irideus) along the Pacific Coast of North America and the inland redband rainbow (O. m. gairdneri) in areas east of the Cascade Mountains in the USA and the Coast Range in British Columbia, Canada. Interest in sport fishing and the ease of hatchery rearing has resulted in a world-wide distribution of the coastal rainbow trout subspecies (Halverson, 2010). Within the United States, stocking practices have distributed the coastal subspecies widely throughout the range of the inland subspecies. The coastal and inland lineages are recognized by differences in coloration and numbers of pyloric caecae, scales along the lateral line, vertebrae and gill rakers (Behnke, 1992). Differences in microsatellite and allozyme frequencies have often been used to study introgression and hybridization between these subspecies (Utter, 2001, Knudsen et al., 2002, Small et al., 2007).
The salmonids are famously known for their anadromy and life history of spawning in fresh water, followed by hatch and juvenile residence in fresh water prior to parr-smolt transformation and oceanic migration. After several years of oceanic maturation, the anadromous form completes this life cycle by precise homing to their natal stream to spawn and, among Pacific salmon, die (Dittman and Quinn, 1996, Quinn, 2005). Homing has lead to reproductive isolation within spawning populations, and selection for adaptations to specific environments. The trouts including O. mykiss are able to optionally remain in fresh water throughout their entire life cycle and survive spawning. Rainbow trout have an ocean-going form (anadromous steelhead) when given access to the sea. Steelhead do not show consistent genetic distinctions from non-migratory resident rainbow trout (McMillan et al., 2007, Narum et al., 2004). Non-anadromous “resident” males, which can mature and spawn without going to sea are common in some populations. Even though the resident males are significantly smaller than the sea-going migrants of the same population, mature resident males contribute successfully during spawning, effectively creating higher homing fidelity (Hendry et al., 2004). In years of low steelhead spawning return, resident precocial parr can sometimes reproductively contribute more than the anadromous form (Seamons et al., 2004).
Previous evaluations of salmonid sex-biased dispersal in migrating and resident populations have yielded mixed results. Male-biased dispersal has been predicted to be a response to reduced mate competition where females are limiting, and this speculation is supported in mark-recapture evaluations of brook trout populations, Salvelinus fontinalis (Hutchings and Gerber, 2002). Evaluations of sex-biased dispersal in rainbow trout (Olsen et al., 2006), and Atlantic salmon do not detect sex-biased dispersal (Consuegra and Garcia de Leaniz, 2007). Conversely, other evaluations of lake-dwelling brook trout sex-biased dispersal have detected a spatial component in which male-mediated gene flow is restricted, while the females are more widely dispersing (Fraser et al., 2004). Female-biased dispersal has also been reported in evaluations of stream-dwelling Dolly Varden (Salvelinus malma) populations (Koizumi et al., 2006).
The recent discovery of a polymorphic Y-linked marker in rainbow trout (Brunelli et al., 2008) has allowed us to study the geographic distribution of this new genetic marker among rainbow trout populations. This marker was initially identified through homology to a sequence isolated in the closely related Chinook salmon (Oncorhynchus tshawytscha) from an AFLP band present in males but not in females (Brunelli and Thorgaard, 2004). Because the male-specific region of the sex chromosome does not recombine it provides an accurate legacy of paternal lineages.
We present the first Y-haplotype phylogeographic evaluation of a fish species. We have found a surprisingly deep divergence between the Y chromosome sequences of inland and coastal rainbow trout populations without a corresponding difference between their mitochondrial DNAs. The difference in patterns between Y markers and mtDNA may be related to differences in dispersal and evolutionary history between the sexes. The two main Y haplotype lineages correspond geographically to the two main subspecies. We also examined mtDNA haplotypes from the same individuals and found that the mtDNA haplotypes do not show the same subspecies associations. Our results suggest that male-specific behaviors may have contributed to the maintenance of subspecific Y haplotypes and that introgression between the subspecies is mediated by females.
Section snippets
Materials and methods
We sampled 333 male rainbow trout (Oncorhynchus mykiss) representing four subspecies (coastal [O. m. irideus], inland [O. m. gairdneri], Kamchatka [O. m. mykiss], and California golden [O. m. aquabonita]) from 57 localities in western North America and Russia (Fig. 1; Supplementary Table 1). Samples from a closely related species, the Apache trout (O. apache), were also included for comparisons. All samples were sequenced for Y-linked and mitochondrial markers (Table 1).
Genomic and
Results
We evaluated the single copy Y-linked OmyY1 marker (Brunelli et al., 2008) for variation over 969 bases from 333 males sampled at 57 localities throughout the natural range of rainbow trout (Fig. 1 and Table 1). This evaluation revealed 13 Y haplotypes. Haplotype networks revealed two distinct haplogroups separated by four mutations (Fig. 2). Each haplogroup generally included individuals from either the inland or coastal subspecies (Fig. 1, Fig. 2). All but three individuals collected from
Discussion
Our results provide the first population-level evaluation of a Y-linked marker in a fish species. Our Y-marker results show the clearest molecular evidence to date supporting the coastal and inland subspecies designations in rainbow trout and suggest different sex-specific evolutionary histories in this species.
Acknowledgments
The authors thank all of the many individuals and agencies who provided the tissue and DNA samples for this study (Supplementary Table 1). Supported by National Institute of Environmental Health Sciences Grant ES012446 to James Nagler, by USDA CSREES National Research Initiative Grants 2006-35205-16728 to Gary Thorgaard and Hubert Schwabl and 2008-04041 to Ruth Phillips and Gary Thorgaard.
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