The evolutionary history of species is a dynamic process as they modify, expand, and contract their spatial distributions over time. Range expansions (REs) occur through a series of founder events that are followed by migration among neighboring demes. The process usually results in structured metapopulations and leaves a distinct signature in the genetic variability of species. Explicitly modeling the consequences of complex demographic events such as REs is computationally very intensive. Here we propose an an alternative approach that requires less computational effort than a comprehensive RE model, but that can recover the demography of species undergoing a RE, by combining spatially explicit modelling with simplified but realistic metapopulation models. We examine the demographic and colonization history of Carcharhinus melanopterus, an abundant reef-associated shark, as a test case. We first used a population genomics approach to statistically confirm the occurrence of a RE in C. melanopterus, and identify its origin in the Indo-Australian Archipelago. Spatial genetic modelling identified two waves of stepping-stone colonization: an eastward wave moving through the Pacific and a westward one moving through the Indian Ocean. We show that metapopulation models best describe the demographic history of this species and that not accounting for this may lead to incorrectly interpreting the observed genetic variation as signals of widespread population bottlenecks. Our study highlights insights that can be gained about demography by coupling metapopulation models with spatial modeling and underscores the need for cautious interpretation of population genetic data when advancing conservation priorities.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $37.75 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Barbujani G, Sokal RR, Oden NL (1995) Indo-European origins: a computer-simulation test of five hypotheses. Am J Phys Anthropol 96:109–132
Beaumont MA (2008) Joint determination of topology, divergence time, and immigration in population trees. In: Matsumura, S., Forster, P. and Renfrew, C. (eds.) Simulation, genetics, and human prehistory. McDonald Institute for Archaeological Research, Cambridge, pp 135–154.
Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162(4):2025–2035
Boitard S, Rodriguez W, Jay F, Mona S, Austerlitz F (2016) Inferring population size history from large samples of genome-wide molecular data—an approximate Bayesian computation approach. PLoS Genet 12:e1005877
Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366
Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558–1561
Chikhi L, Rodriguez W, Grusea S, Santos P, Boitard S, Mazet O (2018) The IICR (inverse instantaneous coalescence rate) as a summary of genomic diversity: insights into demographic inference and model choice. Heredity 120:13–24
Connolly SR, DR B, TP H (2003) Indo-Pacific biodiversity of coral reefs: deviations from a mid-domain model. Ecology 84:2178–2190
Corrigan S, Maisano Delser P, Eddy C, Duffy C, Yang L, Li C et al. (2017) Historical introgression drives pervasive mitochondrial admixture between two species of pelagic sharks. Mol Phylogenet Evol 110:122–126
Cowman P, Parravicini V, Kulbicki M, Floeter S (2017) The biogeography of tropical reef fishes: endemism and provinciality through time Biol Rev Camb Philos Soc 92:2112–2130
Csillery K, Francois O, Blum MGB (2012) abc: an R package for approximate Bayesian computation (ABC). Methods Ecol Evol 3:475–479
Currat M, Excoffier L (2005) The effect of the Neolithic expansion on European molecular diversity. Proc Biol Sci 272(1564):679–688
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al. (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158
Eriksson A, Manica A (2014) The doubly conditioned frequency spectrum does not distinguish between ancient population structure and hybridization. Mol Biol Evol 31:1618–1621
Excoffier L, Dupanloup I, Huerta-Sanchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905
Excoffier L, Foll M, Petit R (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481. 501
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Francois O, Blum MG, Jakobsson M, Rosenberg NA (2008) Demographic history of european populations of Arabidopsis thaliana. PLoS Genet 4:e1000075
Gaggiotti OE, Bekkevold D, Jorgensen HB, Foll M, Carvalho GR, Andre C et al. (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63:2939–2951
Gustafsson F, Gunnarsson F (2003) Positioning using time-difference of arrival measurements. In: 2003 IEEE International Conference on Acoustics, Speech, and Signal Processing, vol VI, Proceedings. pp 553–556
Hamilton G, Currat M, Ray N, Heckel G, Beaumont M, Excoffier L (2005) Bayesian estimation of recent migration rates after a spatial expansion. Genetics 170:409–417
Hanski I (1998) Metapopulation dynamics. Nature 396:41–49
He Q, Prado JR, Knowles LL` (2017) Inferring the geographic origin of a range expansion: Latitudinal and longitudinal coordinates inferred from genomic data in an ABC framework with the program x-origin Mol Ecol 26:6908–6920
Hobbs JPA, Frisch AJ, Allen GR, Van Herwerden L (2009) Marine hybrid hotspot at Indo-Pacific biogeographic border. Biol Lett 5:258–261
Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132(2):583–589
Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475:493–496
López-Garro A, Zanella I, Golfín-Duarte G, Pérez-Montero M (2012) First record of the blacktip reef shark Carcharhinus melanopterus (Carcharhiniformes: Carcharhinidae) from the Tropical Eastern Pacific Rev Biol Trop 6:275–278
Lyle J (1987) Observations on the biology of Carcharhinus cautus (Whitley), C. melanopterus (Quoy & Gaimard) and C. fitzroyensis (Whitley) from Northern Australia. Aust J Mar Freshw Res 38:701–710
Maisano Delser P, Corrigan S, Hale M, Li C, Veuille M, Planes S et al. (2016) Population genomics of C. melanopterus using target gene capture data: demographic inferences and conservation perspectives. Sci Rep 6:33753
Mazet O, Rodriguez W, Chikhi L (2015) Demographic inference using genetic data from a single individual: Separating population size variation from population structure. Theor Popul Biol 104:46–58
Mazet O, Rodriguez W, Grusea S, Boitard S, Chikhi L (2016) On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? Heredity 116:362–371
McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890
Mona S (2017) On the role played by the carrying capacity and the ancestral population size during a range expansion. Heredity 118:143–153
Mona S, Mordret E, Veuille M, Tommaseo-Ponzetta M (2013) Investigating sex-specific dynamics using uniparental markers: West New Guinea as a case study. Ecol Evol 3(8):2647–2660
Mona S, Ray N, Arenas M, Excoffier L (2014) Genetic consequences of habitat fragmentation during a range expansion. Heredity 112:291–299
Mourier J, Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Mol Ecol 22:201–214
Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Anim Behav 83:389–401
Neuenschwander S, Largiader CR, Ray N, Currat M, Vonlanthen P, Excoffier L (2008) Colonization history of the Swiss Rhine basin by the bullhead (Cottus gobio): inference under a Bayesian spatially explicit framework. Mol Ecol 17:757–772
Papastamatiou Y, Friedlander A, Caselle J, Lowe C (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102
Papastamatiou Y, Lowe C, Caselle J, Friedlander A (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008
Peter BM, Slatkin M (2013) Detecting range expansions from genetic data. Evolution 67:3274–3289
Pfeifer B, Wittelsburger U, Ramos-Onsins SE, Lercher MJ (2014) PopGenome: an efficient swiss army knife for population genomic analyses in R. Mol Biol Evol 31:1929–1936
Potter S, Bragg JG, Peter BM, Bi K, Moritz C (2016) Phylogenomics at the tips: inferring lineages and their demographic history in a tropical lizard, Carlia amax. Mol Ecol 25:1367–1380
Quoy JRC, Gaimard JP (1824) Quoy, J. R. C. & J. P. Gaimard, pp 185–232.
Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW, Cavalli-Sforza LL (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102:15942–15947
Ray N, Currat M, Berthier P, Excoffier L (2005) Recovering the geographic origin of early modern humans by realistic and spatially explicit simulations. Genome Res 15:1161–1167
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
R CoreTeam (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Schiffels S, Durbin R (2014) Inferring human population size and separation history from multiple genome sequences. Nat Genet 46:919–925
Schneider N, Chikhi L, Currat M, Radespiel U (2010) Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evol Biol 10:105
Smith S, Au D, Show C (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Mar Freshw Res 49:663–678
Stadler T, Haubold B, Merino C, Stephan W, Pfaffelhuber P (2009) The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics 182:205–216
Stevens J (1984) Life history and ecology of sharks at Aldabra Atoll, Indian Ocean Proc R Soc Lond B Biol Sci 222:79–106
Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Vignaud TM, Mourier J, Maynard JA, Leblois R, Spaet J, Clua E et al. (2014) Blacktip reef sharks, Carcharhinus melanopterus, have high genetic structure and varying demographic histories in their Indo-Pacific range. Mol Ecol 23:5193–5207
Walther BA, Moore JL (2005) The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28:815–829
We are grateful to the genotoul bioinformatics platform Toulouse Midi-Pyrenees (Bioinfo Genotoul) for providing computing resources (www.bioinfo.genotoul.fr). This work was funded by the Agence Nationale de la Recherche Demochips ANR-12-BSV7-0012, a LABEX CORAIL grant to SM and MV (CORALSHARK) and NSF Award DEB-01132229 to GN (Collaborative Research: Jaws and Backbone: Chondrichthyan Phylogeny and a Spine for the Vertebrate Tree of Life). We thank Ornella Weideli and Save Our Seas foundation for providing samples from the Seychelles. We also thank Andrew Chin, Jennifer Ovenden, Mark Meekan and Conrad Speed, Mael Imirizaldu, David Lecchini, Patrick Plantard, Jonathan Werry, Thomas Vignaud, Julia Spät and several students for providing samples or for assistance with blacktip reef shark population genetics sampling. We thank Johann Mourier, Andrea Manica, Anders Eriksson, Robert Beyer and Dave Swofford for helpful discussion.
Conflict of interest
The authors declare that they have no conflict of interest.