Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range

Abstract

In a single well-mixed population, equally abundant neutral alleles are equally likely to persist. However, in spatially complex populations structured by an asymmetric dispersal mechanism, such as a coastal population where larvae are predominantly moved downstream by currents, the eventual frequency of neutral haplotypes will depend on their initial spatial location. In our study of the progression of two spatially separate, genetically distinct introductions of the European green crab (Carcinus maenas) along the coast of eastern North America, we captured this process in action. We documented the shift of the genetic cline in this species over 8 y, and here we detail how the upstream haplotypes are beginning to dominate the system. This quantification of an evolving genetic boundary in a coastal system demonstrates that novel genetic alleles or haplotypes that arise or are introduced into upstream retention zones (regions whose export of larvae is not balanced by import from elsewhere) will increase in frequency in the entire system. This phenomenon should be widespread when there is asymmetrical dispersal, in the oceans or on land, suggesting that the upstream edge of a species' range can influence genetic diversity throughout its distribution. Efforts to protect the upstream edge of an asymmetrically dispersing species' range are vital to conserving genetic diversity in the species.invasive species | marine genetics | phylogeography | physical oceanography N ovel genetic material can appear in a population through mutation, migration, or long-distance dispersal events which may be human-mediated. In a single well-mixed population, the evolution of the frequency of novel neutral alleles will be governed by random genetic drift, not their initial spatial distribution (1). However, spatial structure and complexity can alter this expectation. In a metapopulation linked by migration, alleles introduced into source populations are more likely to persist than those that are introduced into sinks (2-4). Many metapopulations are embedded in complex spatial systems with a preferential direction of migration ("asymmetric dispersal"). In these systems, little is known about the equilibrium frequency of novel alleles or how this frequency depends on the location where these new lineages appear.Asymmetric dispersal is common where propagules are carried long distances by wind or water. In atmospheric, riverine, and oceanic flows, there is usually a predominant flow direction (downstream or downwind) that biases dispersal, and eddies or weather systems that slow or reverse such flow add a stochastic (and potentially upstream) component of migration. For example, many terrestrial plant species have propagules that can be dispersed by the winds (5), and a recent study of the spatial patterns of diversity in moss, liverwort, and lichen flora in the Southern Hemisphere were found to be best explained by the predominantly downwind dispersal (6). Further evidence that asymmetric dispersal can structure a species' genetic patter...

Linking bio-oceanography and population genetics to assess larval connectivity

“…Compared to other systems , the unidirectional flow in the NGC greatly simplifies the identification of source populations, for instance, within a 100 km window capturing demographic connectivity for summer spawners. In such an asymmetric system, upstream populations are predicted to drive patterns of genetic structure throughout the entire area (Pringle et al 2011) and are thus critical for population viability and evolutionary adaptation. Our estimates of genetic connectivity suggest overall uninterrupted gene flow among sampled localities.…”

“…Plantas e invertebrados. FAO, Rome Pringle JM, Blakeslee AMH, Byers JE, Roman J (2011) Asymmetric dispersal allows an upstream region to control population structure throughout a species' range. Proc Natl Acad Sci USA 108: 15288−15293 Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data.…”

Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly distributed marine invasive species, the European green crab,Carcinus maenas

“…Genetic analysis revealed that this rapid northward expansion was concurrent with a second introduction of the species from northern Europe (Roman, 2006). Since that time, the two introduced populations have widely introgressed, with genetic signatures of the original invasion extending throughout the East Coast range, and signatures of the second introduction extending as far south as New York and still moving southward (Pringle et al, 2011). In contrast, the West Coast population was founded circa 1990 by individuals from the original East Coast introduction, and by 1998 had spread to its current distribution between Elkhorn Slough, CA, USA, and Vancouver Island, BC, Canada, with no evidence for multiple introductions (Behrens Yamada et al, 2005;Tepolt et al, 2009).…”

Directional genetic differentiation and relative migration

“…2011), or those with strong habitat quality gradients, which can lead to competition‐driven directional dispersal (Paz‐Vinas et al. 2013).…”

“…2011). For example, when aiming to conserve endangered species, implementing management strategies for source populations is known to be more effective than for sink populations (Dias 1996).…”