Implications for introgression: has selection for fast growth altered the size threshold for precocious male maturation in domesticated Atlantic salmon?

Abstract Background Mature male parr (MMP) represent an important alternative life-history strategy in Atlantic salmon populations. Previous studies indicate that the maturation size threshold for male parr varies among wild populations and is influenced by individual growth, environmental conditions, and genetics. More than ten generations of breeding have resulted in domesticated salmon displaying many genetic differences to wild salmon, including greatly increased growth rates. This may have resulted in domesticated fish with the potential to outgrow the size threshold for early maturation, or evolution of the size threshold of the trait itself. To investigate this, we performed a common-garden experiment under farming conditions using 4680 salmon from 39 families representing four wild, two wild-domesticated hybrid, and two domesticated strains. Results Domesticated salmon outgrew wild salmon 2–5-fold, and hybrids displayed intermediate growth. Overall, the numbers of MMP varied greatly among families and strains: averaging 4–12% in domesticated, 18–25% in hybrid, and 43–74% in the wild populations. However, when the influence of growth was accounted for, by dividing fish into lower and upper size modes, no difference in the incidence of MMP was detected among domesticated and wild strains in either size mode. In the lower size mode, hybrids displayed significantly lower incidences of mature males than their wild parental strains. No consistent differences in the body size of MMP, connected to domestication, was detected. Conclusions Our data demonstrate: 1- no evidence for the evolution of the size threshold for MMP in domesticated salmon, 2- the vastly lower incidence of MMP in domesticated strains under aquaculture conditions is primarily due to their genetically increased growth rate causing them to outgrow the size threshold for early maturation, 3- the incidence of MMP is likely to overlap among domesticated and wild salmon in the natural habitat where they typically display overlapping growth, although hybrid offspring may display lower incidences of mature male parr. These results have implications for wild salmon populations that are exposed to introgression from domesticated escapees

Simulations of genetic drift induced changes between the observed historical genetic profile and computed contemporary populations for each of the six populations displaying temporal genetic change.

<p>Black diamonds represent the mean F_ST between the historical population and the computed contemporary population based upon 1000 simulations of genetic drift with <i>Ne</i> set to 25, 50, 75, 100, 200, 300, 400 and 500. Horizontal black line for each plot represents the observed pair-wise F_ST between the historical and contemporary population (i.e., the values given in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone-0043129-t002" target="_blank">Table 2</a>). “Global” plot represents the global F_ST computed among these six populations based upon the above mentioned simulations, while the horizontal black bar H = historical global F_ST observed among these populations, and C  =  contemporary global F_ST observed among these populations (i.e., the values given in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone-0043129-t003" target="_blank">Table 3</a>). Statistical significance levels for these comparisons are presented in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone-0043129-t005" target="_blank">Table 5</a>.</p

Pair-wise genetic distance as computed by F_ST among the 6 populations displaying the greatest within-river temporal stability.

<p>Computed for historical (bottom left) and contemporary samples (top right), and based upon the analysis of 22 loci.</p><p>All F_ST values significant at α 0.001 with the exception of those in bold.</p

Ratio between global F_ST computed among the 21 contemporary samples divided by the global F_ST computed among the 21 historical samples for 22 microsatellite markers.

<p>Locus number is consequent with locus names and other locus-specific details available in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129.s006" target="_blank">Table S3</a>.</p

Effective population size, within-sample genetic diversity estimates, and temporal genetic stability between historical and contemporary samples within 21 Atlantic salmon rivers located throughout Norway. For full data, including locus specific statistics see Table S2.

<p>Within samples: LD = observed number of deviations from linkage disequilibrium (231 pair-wise tests per population, 211 tests for Opo) at α 0.05, HW = observed deviations from Hardy Weinberg Equilibrium (22 tests per population, 21 tests for Opo) at α 0.05, A_R = allelic richness computed using re-sample size of 25 (note Opo samples only computed with 21 loci therefore not directly comparable to other populations), <i>Ne</i> = effective population size as computed from LD method in LDNE <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Waples1" target="_blank">[90]</a> Inf = Infinity suggesting that the population is “relatively large” (i.e., >200) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Waples2" target="_blank">[93]</a>, # = harmonic mean sample size less than 30 and therefore estimated <i>Ne</i> not to be trusted. Between temporal samples: * = F_ST significant at α 0.05, ** = F_ST significant at α 0.001 (and following Bonferroni), NC = not computed, Exclusion from hist. = percentage of fish from the contemporary population that are excluded from the historical population profile in the program Geneclass at a cut off of α 0.001, temporal change ? = whether significant temporal genetic change is reported within rivers at α 0.001 based upon pair-wise F_ST for both sets of microsatellites.</p

<i>P</i>-values testing whether the observed pair-wise F_ST between each population’s historical and contemporary sample was significantly larger than the F_ST between each population’s observed historical sample and 1000 computer simulated contemporary samples.

<p>Simulations were based upon genetic drift at different <i>Ne</i>. Plots of observed and simulated F_ST values are presented in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone-0043129-g006" target="_blank">Fig. 6</a>.</p

Bayesian clustering of historical (H), intermediate (I) and contemporary (C) samples representing the four rivers displaying the largest temporal genetic changes at 22 microsatellite loci.

<p>For the river Vosso, a total of four samples were available. Thus, the two intermediate samples for this river include a suffix I1 and I2 (linking to these specific samples to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone-0043129-t001" target="_blank">Table 1</a>). These analyses were conducted on each river separately. Inferred ancestry was computed using STRUCTURE v. 2.3.3 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Falush1" target="_blank">[83]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Pritchard1" target="_blank">[84]</a>, under a model assuming admixture and correlated allele frequencies without using population information. Ten runs with a burn-in period consisting of 100000 replications and a run length of 1000000 Markov chain Monte Carlo (MCMC) iterations were performed for a number of clusters ranging from K 1 to 5. Then an ad hoc summary statistic ΔK <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Evanno1" target="_blank">[86]</a> was used to calculate the number of clusters (K) that best fitted the data for each river separately. For full computation details and results for all populations using both 22 and 14 markers see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129.s001" target="_blank">Fig. S1</a> (supporting information).</p

Characteristics of the rivers including catch statistics and numbers of escapees.

<p>Years counted = numbers of years in which farmed salmon were counted in the river, % of farmed salmon = the mean percent of farmed salmon observed in these populations based upon the unweighted mean = average percentage of farmed salmon in spawning population in the period 1989–2009 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-2" target="_blank">[50]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Fiske2" target="_blank">[51]</a>, weighed mean = weighted average percentage of farmed salmon in the population combining data from both sports-fishing and spawning population samples <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-Diserud1" target="_blank">[52]</a>; range for the unweighted mean refers to the lowest and maximum percentages of farmed salmon observed in the spawning populations (this also includes recordings with very low numbers of observations in some years <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-1" target="_blank">[49]</a>). Local stocking history and river catch in 2010 statistics Norway <a href="http://www.ssb.no" target="_blank">www.ssb.no</a>, and 1990 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-3" target="_blank">[125]</a>;</p><p>Na = not available.</p>*<p> = treated against <i>Gyrodactylus salaris</i>;</p>**<p> = Norwegian zone;</p>***<p> = population collapse or strongly reduced;</p><p>smolt and parr stocking activity: <5000 : Low; 5–15000: Medium; >15000: High (eggs, alevins and fry converted to smolt numbers by calculating 10% survival); anadromous area available to smolts <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-1" target="_blank">[49]</a>, and conservation attainment which is the average attainment of the conservation limit for each specific river as defined by the numbers of female salmon left in the river after fishing mortality in relation to the number of eggs required to achieve the rivers estimated carrying capacity <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043129#pone.0043129-1" target="_blank">[49]</a>.</p