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

Abstract

Aim Fractal 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. Location North‐eastern Japan. Methods To 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. Results Our 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 conclusions We 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.

Dispersal behaviour and riverine network connectivity shape the genetic diversity of freshwater amphipod metapopulations

“…In parallel, theoretical models that address the effect of spatial connectivity of riverine networks on genetic variation (Morrissey & de Kerckhove, 2009 ; Paz‐Vinas & Blanchet, 2015 ; Paz‐Vinas et al, 2015 ), on evolution of dispersal (Henriques‐Silva et al, 2015 ), and emergence of neutral genetic structure (Fronhofer & Altermatt, 2017 ; Stokes & Perron, 2020 ; Thomaz et al, 2016 ) have demonstrated that dispersal along riverine networks has a direct imprint on the genetic structure and diversity of the inhabiting organisms. While these theoretical models provide direct testable predictions, a direct comparison between within‐population genetic diversities estimated from empirical data and predictions from theoretical models assuming an identical riverine network has been largely lacking (but see Chiu, Li, et al, 2020 ; Chiu, Nukazawa, et al, 2020 ).…”

Parasite gene flow in riverine habitats: ascertaining the roles of stream drift, river bifurcations and host dispersal

“…By explicitly addressing the effects of dendritic branching on parasite dispersal within river networks, our results highlight that the complexity natural host-parasite systems necessitate future empirical data from natural systems. This foundational knowledge is required to capture the complexity of parasite transmission in river ecosystems within predictive models of both disease spread and parasite adaptive potential within rivers (Thrush et al 2011;Chiu et al 2020;Ma et al 2020). ).…”

“…The spatial hierarchy of the branching networks can be characterized as distal or confluent pathways, which may differentially facilitate decreased or increased dispersal corridors (Chiu et al . 2020).…”

“…The spatial hierarchy of the branching networks can be characterized as distal or confluent pathways, which may differentially facilitate decreased or increased dispersal corridors (Chiu et al 2020). Dispersal asymmetry can also vary spatially within the riverine network, facilitating gene flow along mainstem corridors while distal headwaters may experience less connectivity and subsequent population subdivision and isolation by distance among metapopulations (Alp et al 2012;Thomaz et al 2016).…”

How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale?

“…In the simplest networks, genetic diversity will be lowest in headwater and tributaries and highest at river confluences and on mainstem branches (Thomaz et al 2016). Network models predict increasing complexity in the arrangement of the network will generate increasing genetic diversity, and increased genetic differentiation within the entire river network (Chiu et al 2020). These predictions are empirically supported: effective population size and thus the strength of genetic drift within populations is driven by network properties in fish assemblages (Pilger et al 2017).…”