Veuille Received Feb 19; Accepted Jun 4. Abstract Effective population size Ne is a central evolutionary concept, but its genetic estimation can be significantly complicated by age structure.
Here we investigate Ne in Atlantic salmon Salmo salar populations that have undergone changes in demography and population dynamics, applying four different genetic estimators. For this purpose we use genetic data 14 microsatellite markers from archived scale samples collected between and Through life table simulations we assess the genetic consequences of life history variation on Ne. Although variation in reproductive contribution by mature parr affects age structure, we find that its effect on Ne estimation may be relatively minor.
A comparison of estimator models suggests that even low iteroparity may upwardly bias Ne estimates when ignored semelparity assumed and should thus empirically be accounted for. Our results indicate that Ne may have changed over time in relatively small populations, but otherwise remained stable. Our ability to detect changes in Ne in larger populations was, however, likely hindered by sampling limitations. An evaluation of Ne estimates in a demographic context suggests that life history diversity, density-dependent factors, and metapopulation dynamics may all affect the genetic stability of these populations.
THE effective size of a population Ne is an evolutionary parameter that can be informative on the strength of stochastic evolutionary processes, the relevance of which relative to deterministic forces has been debated for decades e. Stochastic forces include environmental, demographic, and genetic components, the latter two of which are thought to be more prominent at reduced population size, with potentially detrimental consequences for average individual fitness and population persistence Newman and Pilson ; Saccheri et al.
The quantification of Ne in conservation programs is thus frequently advocated e. Effective population size is determined mainly by the lifetime reproductive success of individuals in a population Wright ; Felsenstein Variance in reproductive success, sex ratio, and population size fluctuations can reduce Ne below census population size Frankham Given the difficulty in directly estimating Ne through quantification of these demographic factors reviewed by Caballero , efforts have been directed at inferring Ne indirectly through measurement of its genetic consequences see Leberg , Wang , and Palstra and Ruzzante for reviews.
Studies employing this approach have quantified historical levels of genetic diversity and genetic threats to population persistence e. Ne has been extensively studied in commercially important fish species, due to the common availability of collections of archived samples that facilitate genetic estimation using the temporal method e.
Most models relating Ne to a population's genetic behavior make simplifying assumptions regarding population dynamics. Chiefly among these is the assumption of discrete generations, frequently violated in practice given that most natural populations are age structured with overlapping generations. Here, theoretical predictions still apply, provided that population size and age structure are constant Felsenstein ; Hill Ignored age structure can introduce bias into temporal genetic methods for the estimation of Ne, especially for samples separated by time spans that are short relative to generation interval Jorde and Ryman ; Waples and Yokota ; Palstra and Ruzzante Moreover, estimation methods that do account for age structure e.
Population dynamics will, however, likely be altered as population size changes, thus making precise quantifications of the genetic consequences of acute population declines difficult Nunney ; Engen et al. This problem may be particularly relevant when declines are driven by anthropogenic impacts, such as selective harvesting regimes, that can affect age structure and Ne simultaneously Ryman et al.
Demographic changes thus have broad conservation implications, as they can affect a population's sensitivity to environmental stochasticity and years of poor recruitment Warner and Chesson ; Ellner and Hairston ; Gaggiotti and Vetter Consequently, although there is an urgent need to elucidate the genetic consequences of population declines, relatively little is understood about the behavior of Ne when population dynamics change but see Engen et al.
Here we focus on age structure and Ne in Atlantic salmon Salmo salar river populations in Newfoundland and Labrador. The freshwater habitat in this part of the species' distribution range is relatively pristine Parrish et al.
A fishery moratorium was declared in , with rivers displaying differential recovery patterns since then Dempson et al. An evaluation of those genetic consequences thus requires accounting for potential changes in population dynamics as well as in life history. Life history in Atlantic salmon can be highly versatile Fleming ; Hutchings and Jones ; Fleming and Reynolds , as exemplified by the high variation in age-at-maturity displayed among and within populations Hutchings and Jones , partly reflecting high phenotypic plasticity Hutchings Variability in life history strategies is further augmented by iteroparity, which can be viewed as a bet-hedging strategy to deal with environmental uncertainty e.
Life history diversity and plasticity may allow salmonid fish populations to alter and optimize their life history under changing demography and population dynamics, potentially acting to stabilize Ne.
Reduced variance in individual reproductive success at low breeder abundance genetic compensation will achieve similar effects and might be a realistic aspect of salmonid breeding systems Ardren and Kapuscinski ; Fraser et al. Little is currently known about the relationships between life history plasticity, demographic change and Ne, partly due to scarcity of the multivariate data required for these analyses.
Our objective in this article is twofold. First, we use demographic data for rivers in Newfoundland to quantify how life history variation influences age structure in Atlantic salmon and hence Ne and its empirical estimation from genetic data. We find that variation in reproductive contribution by mature parr has a much smaller effect on the estimation of Ne than is often assumed.
Second, we use temporal genetic data to estimate Ne and quantify the genetic consequences of demographic changes. We attempt to account for potential sources of bias, associated with changes in age structure and life history, by using four different analytical models to estimate Ne: A comparison of results from these different estimators suggests that iteroparity may often warrant analytical consideration, even when it is presumably low.
Although sometimes limited by statistical power, a quantification and comparison of temporal changes in Ne among river populations suggests a more prominent impact of demographic changes on Ne in relatively small river populations. Atlantic salmon life history represents the classical example of anadromy. Juveniles called parr typically spend their first few years in freshwater. They then undergo physiological changes known as smoltification and migrate out to sea at which point they are called smolts.
Anadromous adults, after spending one one-sea winter or grilse or several years multisea winter feeding in the ocean environment, return to spawn in freshwater, typically in the river of origin. Many die after spawning semelparity , but some migrate out to sea again to return and breed again in future years iteroparity.
Alternately, males can mature in freshwater as mature male parr before undertaking any ocean migration. Exceptions are samples consisting of smolts Western Arm Brook, or postspawning adults returning to the sea Northeast Brook Trepassey. Where possible, we pooled samples from 2—3 consecutive years in an attempt to obtain samples representative of the entire population at a given point in time e.