History and extent of introgressive hybridization in Puget Sound rockfishes (Sebastes auriculatus, S. caurinus, and S. maliger)

Thesis (Master's)--University of Washington, 2012Natural hybridization is common in closely related species especially where they invade novel habitat. The patterns of introgressive hybridization are often asymmetrical and are attributed to various influences from selection to gene flow and dispersal. Hybridization has previously been detected in S. auriculatus, S. caurinus, and S. maliger in Puget Sound (the southern Salish Sea) but the details of the history and direction of introgression are incomplete. These Pacific rockfish species are sympatric over most of their geographic range but hybridization has only been detected in Puget Sound. In order to measure interspecific gene flow, we used sequence data from one mitochondrial locus, three nuclear intron loci, and one coding gene to compare interspecific gene flow between collections from the Salish Sea and the Pacific coast. Although ancestral polymorphisms could not be excluded in the analysis of phylogenetic trees, coalescence analysis provided clear evidence for broad-scale, asymmetrical introgression from S. maliger into S. auriculatus and S. caurinus and a much lower incidence of introgression between S. auriculatus and S. caurinus. The absence of F1 hybrids was consistent with historical hybridization events or ongoing, low-level hybridization in the Salish Sea. Although hybrids were found in high frequency, introgressed rockfish in the Salish Sea appear to maintain the morphological characters and coloration of pure parental species morphology. This rockfish hybrid system, with asymmetrical introgression and the maintenance of parental species, may prove useful to study both mechanisms that maintain species boundaries and processes that facilitate speciation

Posterior probability distribution (PPD) for mutation rate scaled splitting time in generations (t) between coastal (Co) and Salish Sea (SS).

<p>The t0 value is the spitting time for <i>S</i>. <i>caurinus</i> and <i>S</i>. <i>maliger</i> and t1 splitting time for <i>S</i>. <i>auriculatus</i> split from <i>S</i>. <i>caurinus</i> and <i>S</i>. <i>maliger</i>.</p

Introgression among three rockfish species (<i>Sebastes</i> spp.) in the Salish Sea, northeast Pacific Ocean

<div><p>Interspecific hybridization is often seen as a major conservation issue, potentially threatening endangered species and decreasing biodiversity. In natural populations, the conservation implications of hybridization depends on both on anthropogenic factors and the evolutionary processes maintaining the hybrid zone. However, the timeline and patterns of hybridization in the hybrid zone are often not known. Therefore, species conservation becomes a concern when recent anthropogenic changes influence hybridization and not if hybridization is part of a long-term process. Here, we use sequence data from one mitochondrial gene, three nuclear introns and one nuclear exon to estimate the direction, geographic extent, frequency and possible timeline of hybridization between three rockfish species (<i>Sebastes auriculatus</i>, <i>S</i>. <i>caurinus</i>, <i>S</i>. <i>maliger</i>) in the Salish Sea, Washington, USA. We show that (i) introgression occurred much more frequently in the Salish Sea than on the outer coast, (ii) introgression was highly asymmetrical from <i>S</i>. <i>maliger</i> into the other two species, (iii) almost 40% of individuals in the Salish Sea were hybrids, with frequency of hybrids increasing with isolation from the coast, and (iv) all hybrids were later generation backcrosses rather than F1 hybrids. Our results suggest long-standing low-level hybridization rather than recent onset of interbreeding because of human induced environmental change, possibly facilitated by specific environmental conditions in the sub-basins of the Salish Sea, and by differences in population sizes during recolonization of the area after the last glaciation. This rockfish hybrid system, with asymmetrical introgression and the maintenance of parental species, may prove useful to study both mechanisms that maintain species boundaries and that facilitate speciation in the presence of rapid environmental change.</p></div

Fish collection localities and sampling regions.

<p>Localities for Salish Sea collection: Red circles are <i>S</i>. <i>maliger</i> (n = 40), purple circles are <i>S</i>. <i>auriculatus</i> (n = 24) and blue circles are <i>S</i>. <i>caurinus</i> (n = 33). Localities for coastal collections (inset): Red circles are <i>S</i>. <i>maliger</i> (n = 17), purple circles are <i>S</i>. <i>auriculatus</i> (n = 13), and blue circles are <i>S</i>. <i>caurinus</i> (n = 12). The size of the shape of the circles are proportional to the size of collection (1–8 individuals). More than one species collected from the same location is represented by adjacent circles. Major basins in the Salish Sea are represented by different colors and the lines at the mouth of each basin approximate locations of a natural, shallow sill. The color fill for each basin corresponds to the number of shallow sills that separate the basin from the outer coast. The sampling areas in the Salish Sea are South Puget Sound (SPS), Hood Canal (HC), Whidbey Basin (WB), and Central Puget Sound (CPS), and North Puget Sound (NPS). NPS includes the Strait of Georgia, San Juan Islands, and the Strait of Juan de Fuca.</p

Population size parameter estimates (q) for <i>S</i>. <i>auriculatus</i>, <i>S</i>. <i>caurinus</i>, and <i>S</i>. <i>maliger</i> and between coastal and Salish Sea populations.

<p>The 95% CI are indicated with bars.</p

Hybrid proportions by region and species.

<p>Hybrid proportions by region and species.</p

Posterior probability distribution (PPD) for estimated effective number of migrants (2NM) between species for the coastal and Salish Sea populations.

<p>Species are coded by two letters: Sa–<i>S</i>. <i>auriculatus</i>, Sc–<i>S</i>. <i>caurinus</i>, Sm–<i>S</i>. <i>maliger</i>. The PPD highest peak values are posted above the distribution.</p

Ancestry coefficient (Q) from <i>structure</i> analysis for each individual to one of three genetic groups (k = 3).

<p>Each vertical bar represents a single individual and the colors shows the proportion of ancestry to each genetic group. The three genetic clusters are represented by purple as <i>S</i>. <i>auriculatus</i>, blue as <i>S</i>. <i>caurinus</i> and red as <i>S</i>. <i>maliger</i>. The results for each individual are arranged vertically by morphological species and population: 1 = <i>S</i>. <i>auriculatus</i> (coast), 2 = <i>S</i>. <i>auriculatus</i> (Salish Sea), 3 = <i>S</i>. <i>caurinus</i> (coast), 4 = <i>S</i>. <i>caurinus</i> (Salish Sea), 5 = <i>S</i>. <i>maliger</i> (Salish Sea), 6 = <i>S</i>. <i>maliger</i> (Salish Sea); A and B are <i>S</i>. <i>caurinus</i> hybrid whole specimens from SPS, and C is the <i>S</i>. <i>caurinus</i> putative hybrid whole specimen from CPS. The samples are approximately sorted from left to right on the figure by geography north to south.</p

DNA polymorphism data for five genes across three species each with two populations.

<p>DNA polymorphism data for five genes across three species each with two populations.</p

Locus data.

<p>Locus data.</p