Deep divergence and apparent sex-biased dispersal revealed by a Y-linked marker in rainbow trout

https://doi.org/10.1016/j.ympev.2010.05.016Get rights and content

Abstract

Y-chromosome and mitochondrial DNA markers can reveal phylogenetic patterns by allowing tracking of male and female lineages, respectively. We used sequence data from a recently discovered Y-linked marker and a mitochondrial marker to examine phylogeographic structure in the widespread and economically important rainbow trout (Oncorhynchus mykiss). Two distinct geographic groupings that generally correspond to coastal and inland subspecies were evident within the Y-marker network while the mtDNA haplotype network showed little geographic structure. Our results suggest that male-specific behavior has prevented widespread admixture of Y haplotypes and that gene flow between the coastal and inland subspecies has largely occurred through females. This new Y marker may also aid conservation efforts by genetically identifying inland populations that have not hybridized with widely stocked coastal-derived hatchery fish.

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.

References (48)

  • K.H. Brown et al.

    Genetic analysis of interior Pacific Northwest Oncorhynchus mykiss reveals apparent ancient hybridization with westslope cutthroat trout

    Trans. Am. Fish. Soc.

    (2004)
  • J.P. Brunelli et al.

    A new Y-chromosome-specific marker for Pacific salmon

    Trans. Am. Fish. Soc.

    (2004)
  • J.P. Brunelli et al.

    Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon

    Genome

    (2008)
  • J.F. Coldes et al.

    Identifying introgressive hybridization in native populations of California golden trout based on molecular markers

    Trans. Am. Fish. Soc.

    (2006)
  • S. Consuegra et al.

    Fluctuating sex ratios, but no sex-biased dispersal in a promiscuous fish

    Evol. Ecol.

    (2007)
  • K.P. Currens et al.

    Evolutionary ecology of redband trout

    Trans. Am. Fish. Soc.

    (2009)
  • R.G. Danzmann et al.

    A major sextet of mitochondrial DNA phylogenetic assemblages extant in eastern North American brook trout (Salvelinus fontinalis): distribution and postglacial dispersal patterns

    Can. J. Zool.

    (1998)
  • A.H. Dittman et al.

    Homing in pacific salmon: mechanisms and ecological basis

    J. Exp. Biol.

    (1996)
  • J. Eriksson et al.

    Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus)

    Mol. Ecol.

    (2006)
  • L. Excoffier et al.

    Arlequin ver. 3.0: an integrated software package for population genetics data analysis

    Evol. Bioinform. Online

    (2005)
  • D.J. Fraser et al.

    Consequences of unequal population size, asymmetric gene flow and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis)

    Mol. Ecol.

    (2004)
  • S.L. Graziano et al.

    Nomenclature of mitochondrial DNA haplotypes for Oncorhynchus mykiss

    Trans. Am. Fish. Soc.

    (2005)
  • A. Halverson

    An Entirely Synthetic Fish

    (2010)
  • A.P. Hendry et al.

    To sea or not to sea: anadromy versus non-anadromy in salmonids

  • Cited by (0)

    View full text