Is the central-marginal hypothesis a general rule? Evidence from three distributions of an expanding mangrove species, Avicennia germinans (L.) L.

John Paul Kennedy,Ilka C Feller,Richard F Preziosi,Jennifer K Rowntree

doi:10.1111/mec.15365

Abstract

The central‐marginal hypothesis (CMH) posits that range margins exhibit less genetic diversity and greater inter‐population genetic differentiation compared to range cores. CMH predictions are based on long‐held “abundant‐centre” assumptions of a decline in ecological conditions and abundances towards range margins. Although much empirical research has confirmed CMH, exceptions remain almost as common. We contend that mangroves provide a model system to test CMH that alleviates common confounding factors and may help clarify this lack of consensus. Here, we document changes in black mangrove (Avicennia germinans) population genetics with 12 nuclear microsatellite loci along three replicate coastlines in the United States (only two of three conform to underlying “abundant‐centre” assumptions). We then test an implicit prediction of CMH (reduced genetic diversity may constrain adaptation at range margins) by measuring functional traits of leaves associated with cold tolerance, the climatic factor that controls these mangrove distributional limits. CMH predictions were confirmed only along the coastlines that conform to “abundant‐centre” assumptions and, in contrast to theory, range margin A. germinans exhibited functional traits consistent with greater cold tolerance compared to range cores. These findings support previous accounts that CMH may not be a general rule across species and that reduced neutral genetic diversity at range margins may not be a constraint to shifts in functional trait variation along climatic gradients.

Highlights

Understanding factors that control species distributional limits is a central objective in ecology (Gaston, 2009; Hardie & Hutchings, 2010), and necessary insight to better predict responses to climate change (Chen, Hill, Ohlemüller, Roy, & Thomas, 2011)
We test an implicit prediction of central-marginal hypothesis (CMH) by measuring functional traits of leaves associated with cold tolerance, the climatic factor that controls these mangrove distributional limits
An absence of extreme freezes since the late 1980s is linked to ongoing, rapid range expansion of A. germinans into salt marsh habitat at all United States (USA) northern limits, in Texas (Armitage, Highfield, Brody, & Louchouarn, 2015; Everitt, Yang, Judd, & Summy, 2010), Louisiana (Osland, Day, et al, 2017), West Florida (Saintilan et al, 2014; Stevens, Fox, & Montague, 2006), and East Florida (Cavanaugh et al, 2014; Rodriguez et al, 2016), with further proliferation at, and expansion past, these range margins forecast with climate change (Cavanaugh et al, 2015; Osland, Day, et al, 2017; Osland, Enwright, Day, & Doyle, 2013)

Summary

| INTRODUCTION

Understanding factors that control species distributional limits is a central objective in ecology (Gaston, 2009; Hardie & Hutchings, 2010), and necessary insight to better predict responses to climate change (Chen, Hill, Ohlemüller, Roy, & Thomas, 2011). An absence of extreme freezes since the late 1980s is linked to ongoing, rapid range expansion of A. germinans into salt marsh habitat at all USA northern limits, in Texas (Armitage, Highfield, Brody, & Louchouarn, 2015; Everitt, Yang, Judd, & Summy, 2010), Louisiana (Osland, Day, et al, 2017), West Florida (Saintilan et al, 2014; Stevens, Fox, & Montague, 2006), and East Florida (Cavanaugh et al, 2014; Rodriguez et al, 2016), with further proliferation at, and expansion past, these range margins forecast with climate change (Cavanaugh et al, 2015; Osland, Day, et al, 2017; Osland, Enwright, Day, & Doyle, 2013) This wealth of previous research demonstrates that USA mangroves simplify tests of CMH as parallel gradients in latitude, ecological marginality (in terms of minimum temperatures), and postglacial recolonization exist along each of these three distribution ranges. Along each of the three distribution ranges, we asked: (a) Does neutral intrapopulation genetic diversity decrease towards range margins?; (b) Does interpopulation genetic differentiation increase towards range margins?; (c) Do functional traits of leaves exhibit changes consistent with greater cold tolerance towards range margins?

| MATERIALS AND METHODS

Findings

| DISCUSSION