Branching networks can have opposing influences on genetic variation in riverine metapopulations

Ming‐Chih Chiu,Vincent H Resh,Kei Nukazawa,Thaddeus Carvajal,Kozo Watanabe,Bin Li

doi:10.1111/ddi.13160

Abstract

AbstractAimFractal networks, represented by branching complexity in rivers, are ubiquitous in nature. In rivers, the number of either distal (e.g. in headwater streams) or confluent (e.g. in mainstems) locations can be increased along with their branching complexity. Distal‐ or confluent‐spatial locations can result in fewer or greater corridor linkages that can alter genetic divergence at the metapopulation scale. These mechanisms underlying the resulting genetic structuring remain poorly understood at the metapopulation scale, particularly in terms of the roles of species‐specific dispersal traits. The objective of this study was to mechanistically understand how branching complexity can simultaneously influence genetic divergence in opposite directions.LocationNorth‐eastern Japan.MethodsTo evaluate the integrated influences of network complexity and species dispersal on genetic divergence among populations at the catchment scale, we modelled metapopulation genetic dynamics under a Bayesian inference framework by adapting empirical genetic data from four macroinvertebrate species. Simulations were then performed using empirical and virtual species characteristics on virtual river networks.ResultsOur simulation experiments showed that both greater landscape connectivity (resulting from shorter watercourse distance) and greater isolation of distal locations occurred in the more‐branched river networks. These two spatial features have negative and positive influences on genetic divergence, with their relative importance varying among different species and dispersal characteristics. Specifically, genetic divergence at the metapopulation scale increased for species having higher downstream‐biased dispersal but decreased for species having higher upstream‐biased dispersal. Distal populations (e.g. in headwaters) have higher genetic independence when downstream‐biased asymmetry is higher.Main conclusionsWe found a strong association between species dispersal and evolutionary processes such as gene flow and genetic drift. This association mediates the pervasive influences of branching complexity on genetic divergence in the metapopulation. It also highlights the importance of considering species dispersal patterns when developing management strategies in the face of rapid environmental change scenarios.

Highlights

There is increasing interest in understanding how landscape architecture determines spatial patterns of intraspecific genetic-diversity (Paz-Vinas, Loot, Stevens, & Blanchet, 2015; Phillipsen & Lytle, 2013), a mechanistic understanding of this process remains highly challenging in the real world
Landscape connectivity shapes evolutionary processes, such as gene flow and genetic drift, which produce the spatial patterns observed in intraspecific genetic variation (McRae, 2006; Phillipsen et al, 2015; Thomaz et al, 2016)
By using a mechanistic model based on evolutionary processes and asymmetric dispersal, we explored the spatial genetic variation among four macroinvertebrate species with flying adult-stages that occur in a river network of northeastern Japan

Summary

Introduction

There is increasing interest in understanding how landscape architecture determines spatial patterns of intraspecific genetic-diversity (Paz-Vinas, Loot, Stevens, & Blanchet, 2015; Phillipsen & Lytle, 2013), a mechanistic understanding of this process remains highly challenging in the real world. More in-depth explorations of the integrated genetic effects of species dispersal and landscape connectivity on metapopulations (here defined as groups of subpopulations with dispersal interactions) occurring in complex habitats are needed These efforts are especially important when fragmented landscapes that result from global-change influences affect spatial genetic variability (Martins et al, 2016; Prunier, Dubut, Loot, Tudesque, & Blanchet, 2018). Fractal branching-networks (e.g., those with “treelike” patterns) have similar structural features to those seen in fluvial landscapes (Green, Klomp, Rimmington, & Sadedin, 2006) In these environments, landscape connectivity shapes evolutionary processes, such as gene flow and genetic drift, which produce the spatial patterns observed in intraspecific genetic variation (McRae, 2006; Phillipsen et al, 2015; Thomaz et al, 2016). In analyzing the evolutionary action of landscape architecture, branching networks can be characterised by being either distal or confluent locations (e.g., in headwater streams or mainstems, respectively), which allow fewer or greater corridor linkages, respectively

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