Oceanographic connectivity explains the intra-specific diversity of mangrove forests at global scales

Abstract

The distribution of mangrove intra-specific biodiversity can be structured by historical demographic processes that enhance or limit effective population sizes. Oceanographic connectivity (OC) may further structure intra-specific biodiversity by preserving or diluting the genetic signatures of historical changes. Despite its relevance for biogeography and evolution, the role of oceanographic connectivity in structuring the distribution of mangrove’s genetic diversity has not been addressed at global scale. Here we ask whether connectivity mediated by ocean currents explains the intra-specific diversity of mangroves. A comprehensive dataset of population genetic differentiation was compiled from the literature. Multigenerational connectivity and population centrality indices were estimated with biophysical modeling coupled with network analyses. The variability explained in genetic differentiation was tested with competitive regression models built upon classical isolation-by-distance (IBD) models considering geographic distance. We show that oceanographic connectivity can explain the genetic differentiation of mangrove populations regardless of the species, region, and genetic marker (significant regression models in 95% of cases, with an average R-square of 0.44 ± 0.23 and Person’s correlation of 0.65 ± 0.17), systematically improving IBD models. Centrality indices, providing information on important stepping-stone sites between biogeographic regions, were also important in explaining differentiation (R-square improvement of 0.06 ± 0.07, up to 0.42). We further show that ocean currents produce skewed dispersal kernels for mangroves, highlighting the role of rare long-distance dispersal events responsible for historical settlements. Overall, we demonstrate the role of oceanographic connectivity in structuring mangrove intra-specific diversity. Our findings are critical for mangroves’ biogeography and evolution, but also for management strategies considering climate change and genetic biodiversity conservation.

Unravelling the role of oceanographic connectivity in intra-specific diversity of marine forests at global scale

“…To evaluate the impact of such functions, we also generate an additional square matrix using a fixed dispersal time of 7.43 d (i.e., the mean of dispersal range time for in-house dispersal capacity). This matrix only considered trajectories with a dispersal duration equal to or less than this fixed time, without any weighting process, as commonly implemented elsewhere (e.g., Gouvêa et al, 2023, Legrand et al, 2019, 2022.…”

“…On top of that, contemporary gene flow between established populations can homogenise allele frequencies, reshuffle mutations, disperse adaptive changes, and mitigate the effects of inbreeding depression (Hellberg, 2009, Lenormand et al, 2002. However, deciphering the relative contribution of present-day connectivity from historical processes on observed genetic structures remains a major challenge, with attempts at the global scale limited to a few species (e.g., mangrove forests; Gouvêa et al, 2023) and regions (e.g., Mediterranean Sea; Legrand et al, 2022).…”

“…Most studies focused on the genetic drivers of marine forests have inferred the contribution of presentday connectivity through observed patterns of population genetic differentiation (Maggs et al, 2008) or through isolation by distance models (Riquet et al, 2021). These simplistic approaches cannot capture the complexity of ongoing oceanographic processes (Jahnke et al, 2022), which can produce asymmetrical population gene flow with high temporal and spatial variability (Gouvêa et al, 2023, Legrand et al, 2022. The few studies considering mechanistic biophysical modelling mimicking oceanographic processes over multiple generations are limited to few species (e.g., Cystoseira amentacea, Fucus radicans, Fucus vesiculosus, Laminaria ochroleuca and Laminaria pallida) and realms (e.g., Temperate Northern Atlantic and Temperate Southern Africa; Spalding et al, 2007) and have never integrated LDD (Assis et al, 2018, 2022, Buonomo et al, 2017, Pereyra et al, 2013, precluding conclusions on the relative contribution of present-day oceanographic connectivity on marine forests' genetic structures.…”

Population genetic structure of Kawakawa (Euthynnus affinis Cantor, 1849) in Malaysian waters based on COI gene

“…The findings of this study indicate a potential decrease in the exchange of genetic material between the studied locations, most probably caused by oceanic currents (Halim et al 2022). Oceanic currents can affect gene flow among regions by creating barriers that isolate populations and increase differentiation levels or promoting long-distance dispersal (Gouvêa et al 2023). The direction and strength of ocean currents can influence the movement of marine species and their larvae, which affects the distribution of genetic variation among populations (Snead et al 2023).…”

Range wide genetic differentiation in the bull kelp Nereocystis luetkeana with a seascape genetic focus on the Salish Sea

“…This suggests that ocean currents affect the Salish Sea more directly in the Juan de Fuca and Georgia Straits than in Puget Sound. The importance of oceanographic currents as a driver of gene flow has been found across a variety of marine dispersed taxa, including other kelps (White et al, 2010;Alberto et al, 2011;Truelove et al, 2017;Wesselmann et al, 2018;Xuereb et al, 2018;Gouveâ et al, 2023).…”