Contemporary effective population and metapopulation size (Ne and meta-Ne): comparison among three salmonids inhabiting a fragmented system and differing in gene flow and its asymmetries

We estimated local and metapopulation effective sizes ( and meta-) for three coexisting salmonid species (Salmo salar, Salvelinus fontinalis, Salvelinus alpinus) inhabiting a freshwater system comprising seven interconnected lakes. First, we hypothesized that might be inversely related to within-species population divergence as reported in an earlier study (i.e., FST: S. salar> S. fontinalis> S. alpinus). Using the approximate Bayesian computation method implemented in ONeSAMP, we found significant differences in () between species, consistent with a hierarchy of adult population sizes (). Using another method based on a measure of linkage disequilibrium (LDNE: ), we found more finite values for S. salar than for the other two salmonids, in line with the results above that indicate that S. salar exhibits the lowest among the three species. Considering subpopulations as open to migration (i.e., removing putative immigrants) led to only marginal and non-significant changes in , suggesting that migration may be at equilibrium between genetically similar sources. Second, we hypothesized that meta- might be significantly smaller than the sum of local s (null model) if gene flow is asymmetric, varies among subpopulations, and is driven by common landscape features such as waterfalls. One ‘bottom-up’ or numerical approach that explicitly incorporates variable and asymmetric migration rates showed this very pattern, while a number of analytical models provided meta- estimates that were not significantly different from the null model or from each other. Our study of three species inhabiting a shared environment highlights the importance and utility of differentiating species-specific and landscape effects, not only on dispersal but also in the demography of wild populations as assessed through local s and meta-s and their relevance in ecology, evolution and conservation.

[1]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[2]  S. J. Arnold,et al.  Population genetic analysis identifies source–sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis) , 2005, Molecular ecology.

[3]  L. Nunney.  THE EFFECTIVE SIZE OF A HIERARCHICALLY STRUCTURED POPULATION , 1999, Evolution; international journal of organic evolution.

[4]  R. Walter,et al.  Gene flow increases temporal stability of Chinook salmon (Oncorhynchus tshawytscha) populations in the Upper Fraser River, British Columbia, Canada , 2009 .

[5]  D. Gomez-Uchida,et al.  Genetic divergence between sympatric Arctic charr Salvelinus alpinus morphs in Gander Lake, Newfoundland: roles of migration, mutation and unequal effective population sizes , 2008 .

[6]  F. Rousset.  Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. , 1997, Genetics.

[7]  G. Fader,et al.  A conceptual model of the deglaciation of Atlantic Canada , 2006 .

[8]  William G. Hill,et al.  Estimation of effective population size from data on linkage disequilibrium , 1981 .

[9]  P. Parker,et al.  Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.) , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  J. Cornuet,et al.  GENECLASS2: a software for genetic assignment and first-generation migrant detection. , 2004, The Journal of heredity.

[11]  D. Coltman,et al.  The effects of cyclic dynamics and mating system on the effective size of an island mouflon population , 2007, Molecular ecology.

[12]  G. Luikart,et al.  Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches , 2010, Conservation Genetics.

[13]  R. Waples,et al.  A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci* , 2006, Conservation Genetics.

[14]  F. Palstra,et al.  Demographic and genetic factors shaping contemporary metapopulation effective size and its empirical estimation in salmonid fish , 2011, Heredity.

[15]  L. Bernatchez,et al.  Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems , 2007, Molecular ecology.

[16]  Jinlian Wang,et al.  Estimation of effective population sizes from data on genetic markers , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  F. Allendorf,et al.  Ecological and life history characteristics predict population genetic divergence of two salmonids in the same landscape , 2004, Molecular ecology.

[18]  L. Bernatchez,et al.  Consequences of unequal population size, asymmetric gene flow and sex‐biased dispersal on population structure in brook charr (Salvelinus fontinalis) , 2004, Molecular ecology.

[19]  H. Robison,et al.  LIFE‐HISTORY VARIATION AND COMPARATIVE PHYLOGEOGRAPHY OF DARTERS (PISCES: PERCIDAE) FROM THE NORTH AMERICAN CENTRAL HIGHLANDS , 1996, Evolution; international journal of organic evolution.

[20]  F. Palstra,et al.  Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? , 2008, Molecular ecology.

[21]  K. Hindar,et al.  Effective size in management and conservation of subdivided populations. , 2003, Journal of theoretical biology.

[22]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[23]  Lennart Persson,et al.  Culling Prey Promotes Predator Recovery — Alternative States in a Whole-Lake Experiment , 2022 .

[24]  G. Luikart,et al.  COMPUTER PROGRAMS: onesamp: a program to estimate effective population size using approximate Bayesian computation , 2008, Molecular ecology resources.

[25]  B. Rannala,et al.  Detecting immigration by using multilocus genotypes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Wright,et al.  Isolation by distance under diverse systems of mating. , 1946, Genetics.

[27]  D. Couvet,et al.  Estimation of effective population size and migration rate from one- and two-locus identity measures. , 2001, Genetics.

[28]  M. Whitlock,et al.  Estimating effective population size and migration rates from genetic samples over space and time. , 2003, Genetics.

[29]  D. Gomez-Uchida,et al.  Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids , 2009, Molecular ecology.

[30]  G. Moyer,et al.  Linkage disequilibrium and effective population size when generations overlap , 2012, Evolutionary applications.

[31]  T. Maruyama,et al.  Analysis of population structure , 1970, Human Population Genomics.

[32]  F. Palstra,et al.  Age Structure, Changing Demography and Effective Population Size in Atlantic Salmon (Salmo salar) , 2009, Genetics.

[33]  M. Whitlock,et al.  The effective size of a subdivided population. , 1997, Genetics.

[34]  R. Waples.  Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? , 2005, Molecular ecology.

[35]  S. Wright.  THE INTERPRETATION OF POPULATION STRUCTURE BY F‐STATISTICS WITH SPECIAL REGARD TO SYSTEMS OF MATING , 1965 .

[36]  Arnaud Estoup,et al.  Genetic assignment methods for the direct, real‐time estimation of migration rate: a simulation‐based exploration of accuracy and power , 2004, Molecular ecology.

[37]  I. Koizumi,et al.  Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream‐dwelling Dolly Varden charr , 2006, Molecular ecology.

[38]  Armando Caballero,et al.  Developments in predicting the effective size of subdivided populations , 1999, Heredity.

[39]  D. Weetman,et al.  Concordant Genetic Estimators of Migration Reveal Anthropogenically Enhanced Source-Sink Population Structure in the River Sculpin, Cottus gobio , 2006, Genetics.

[40]  T. Maruyama.  Analysis of population structure: II. Two‐dimensional stepping sone models of finite length and other geographically structured populations * , 1971 .

[41]  K. Hindar,et al.  Effective size of an Atlantic salmon (Salmo salar L.) metapopulation in Northern Spain , 2009, Conservation Genetics.

[42]  P. England,et al.  Estimating Contemporary Effective Population Size on the Basis of Linkage Disequilibrium in the Face of Migration , 2011, Genetics.

[43]  N. Yamamura,et al.  How to compute the effective size of spatiotemporally structured populations using separation of time scales. , 2007, Theoretical population biology.

[44]  J. E. Byers,et al.  Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range , 2011, Proceedings of the National Academy of Sciences.

[45]  L. Waits,et al.  Monitoring the effective population size of a brown bear (Ursus arctos) population using new single‐sample approaches , 2012, Molecular ecology.

[46]  J. Garza,et al.  Detection of reduction in population size using data from microsatellite loci , 2001, Molecular ecology.

[47]  R. Lande.  Genetics and demography in biological conservation. , 1988, Science.

[48]  R. Waples,et al.  Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution , 2009, Evolutionary applications.

[49]  R. Waples,et al.  ldne: a program for estimating effective population size from data on linkage disequilibrium , 2008, Molecular ecology resources.

[50]  N. Catto,et al.  Topographically-controlled Deglacial History of the Humber River Basin, Western Newfoundland , 2003 .

[51]  T. Beebee,et al.  A comparison of single‐sample effective size estimators using empirical toad (Bufo calamita) population data: genetic compensation and population size‐genetic diversity correlations , 2009, Molecular ecology.

[52]  W. R. Ardren,et al.  Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout , 2002, Molecular ecology.

[53]  A. Finstad,et al.  The Relevance of Individual Size to Management of Arctic Charr, Salvelinus Alpinus, Populations , 2004, Environmental Biology of Fishes.

[54]  S. J. Arnold,et al.  Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[55]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.

[56]  V. Loeschcke,et al.  Conservation Genetics , 2019, Handbook of Statistical Genomics.