Rapid diversification of gray mangroves ( Avicennia  marina ) driven by geographic isolation and extreme environmental conditions  in the Arabian Peninsula

Running title: Evolution of Arabian mangrovesGuillermo Friis*, Edward G. Smith, Catherine E. Lovelock, Alejandra Ortega, Alyssa Marshell, Carlos M. Duarte, John A. Burt*Corresponding author: Center for Genomics and Systems Biology, New York University — Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates; Email: guillefriis@gmail.com; Tel: +97126286739. AbstractBiological systems occurring in ecologically heterogeneous and spatially discontinuous habitats provide an ideal opportunity to investigate the relative roles of neutral and selective factors in driving lineage diversification. The gray mangroves (Avicennia marina) of Arabia occur at the northern edge of the species’ range and are subject to variable, often extreme, environmental conditions, as well as historic large fluctuations in habitat availability and connectivity resulting from Quaternary glacial cycles. Here, we analyze fully sequenced genomes sampled from 19 locations across the Red Sea, the Arabian Sea and the Persian/Arabian Gulf (PAG) to reconstruct the evolutionary history of the species in the region, and to identify adaptive mechanisms of lineage diversification. Population structure and phylogenetic analyses revealed marked genetic structure correlating with geographic distance and highly supported clades among and within the seas surrounding the Arabian Peninsula. Demographic modelling showed times of divergence consistent with recent periods of geographic isolation and low marine connectivity during glaciations, suggesting the presence of (cryptic) glacial refugia in the Red Sea and the PAG. Significant migration was detected within the Red Sea and the PAG, and across the Strait of Hormuz to the Arabian Sea, suggesting gene flow upon secondary contact among populations. Genetic‐environment association analyses revealed high levels of adaptive divergence, and detected signs of multi-loci local adaptation driven by temperature extremes and hypersalinity. These results support a process of rapid diversification resulting from the combined effects of historical factors and ecological selection, and reveal mangrove peripheral environments as relevant drivers of lineage diversity.IntroductionLineage diversification involves both neutral and selective factors, and elucidating their relative roles in the process of evolutionary divergence is essential to understand the mechanisms underlying the early stages of speciation (Coyne & Orr, 2004; Nosil, 2012). Evolutionary divergence may result from the accumulation of genetic differences caused by drift in geographic isolation or isolation-by-distance (IBD, Wright, 1943, 1946), a mode of divergence driven by neutral factors (Mayr, 1954, 1963). In turn, geographic variation in environmental conditions can result in divergent selection, the diversifying process that drives ecological speciation (Coyne & Orr, 2004; Darwin, 1859; Nosil, 2012). In ecological speciation models, reproductive barriers arise as a by-product of cumulative, ecologically adaptive changes (Mayr, 1947; Rundle & Nosil, 2005; Schluter, 2000), enabling genome‐wide differentiation at both neutral and selected loci (Funk, Egan, & Nosil, 2011; Nosil, Egan, & Funk, 2008; Shafer & Wolf, 2013; Wang & Bradburd, 2014). Ecological speciation in geographic isolation is theoretically uncontroversial, and deemed common in nature as a mechanism maintaining lineage diversity upon secondary contact (Keller & Seehausen, 2012; Nosil, 2012; Rundle & Nosil, 2005). However, whether environment-driven processes of lineage diversification occur frequently in nature in the absence of long-term geographic isolation and reduced gene flow remains debated in evolutionary research (Bolnick & Fitzpatrick, 2007; Fitzpatrick, Fordyce, & Gavrilets, 2008; Foote, 2018). The interactions between selection and the stochastic effects derived from processes such as founder events, bottlenecks and genetic drift also remain unclear, and difficult to assess in natural systems (Barton & Charlesworth, 1984; Burri et al., 2015; Kliber & Eckert, 2005). Biological systems occurring at the species' range edges, which are frequently extreme and environmentally diverse habitats, are suitable models to investigate questions related to lineage diversification. The environment at the edges of species’ range tends to be stressful and spatially discontinuous, as well as temporally unstable (Lesica & Allendorf, 1995), often resulting in dynamic settings of multiple isolated populations subject to strong differential selection. The severe and stochastic character of peripheral environments is hypothesized to generate strong selective interplay between adaptation and neutral processes (Hardie & Hutchings, 2010), providing an ideal opportunity for speciation research. One such system is provided by gray mangrove populations in the Arabian Peninsula (Avicennia marina var. marina). The gray mangrove has the broadest distribution of any mangrove species (Hogarth, 2015; Spalding, Kainuma, & Collins, across the and the as as and New & 2015; et al., et al., and to their habitat which a for the of and in selection and & 2013; et al., The Arabian Peninsula of the edges of the species’ distribution et al., as well as a stressful habitat by extreme and often extreme factors to be for mangrove Lovelock, & & Arabian marine are also environmentally diverse both and the the which the Red Sea, the marine system of and with the temperature and in the has high as a result of and high et al., & the Persian/Arabian Gulf to as to the of the Arabian populations are subject to to and the range of in the the & and the Arabian Sea and Sea of which in with has and that are by as a result of the resulting in environmental conditions The Arabian Peninsula has large fluctuations in and environmental conditions that the of the region, in the of the Red Sea and the et al., the the Red Sea has to the the Strait of that at times of glacial as low as of that resulting in in and temperature within the Red Sea as well as isolation at times et al., periods during the glacial the the Red Sea to the Arabian Sea was and the local levels levels et al., In models that the was during the of the marine the the northern the with the In as an the Arabian Sea has migration of levels during glacial geographic The of extreme environmental conditions, differential changes in habitat and dynamic barriers to gene the seas the Arabian Peninsula of the marine environments in the with a high for speciation driven by both neutral and selective factors et al., the phylogenetic for the of A. marina and species for & et al., & the gray mangrove populations from the Arabian in analyses & et al., et al., & 2000), that their evolutionary and remain The drivers and of local adaptation and lineage diversification in A. marina also remain both in Arabia and across Here, we the Arabian gray mangrove to extreme habitat conditions and heterogeneous settings genetic diversity at the highly edge of the species’ range and environmental we of structure and the evolutionary and history of the species in the Arabian Peninsula. the evolutionary history of the Arabian mangroves in mangroves from the Red Sea and during the glacial of the by a the glacial and mangroves within the seas in glacial refugia during glacial and levels we of adaptive association environmental and to the and identify environmental and in local adaptation and lineage and sampled a of of marina from 19 of the Arabian Peninsula and from to be as was from by at and in for to for of the was from the to the and with to and sequenced in a of resulting in a and of was by with & and was with resulting in a of between and the for A. marina et al., the in the & and with marked also with the from the et al., to a of in the et al., we of a range of between and or with a a of at of and et al., 2013; 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The analyses also showed genetic differentiation between the populations from the the and the of the of the Red as well as between the northern and of the PAG. levels of between the populations of the and the Sea of also suggesting lineage or gene flow between revealed a between neutral genetic differentiation and geographic distance among populations. However, a showed of genetic distance that with geographic a was among populations within the Red Sea and the PAG, was across suggesting that drift has gene flow of genetic differentiation at and between of populations by geographic barriers & of of and to within and between in the PAG, suggesting of isolation from geographic distance also within These results support the of in the differentiation of mangrove also that geographic barriers to gene flow to differentiation at geographic However, barriers are the geographic distribution of the Arabian between and divergence in isolated populations is in revealed a of among Arabian mangrove and phylogenetic occurring in the Red Sea, the Arabian Sea and the PAG, with the the populations of the Sea of of phylogenetic divergence among Arabian for marine et al., et al., et al., 2015; et al., Smith, & with the geographic distribution of the species and with barriers to gene flow et al., et al., However, marine in Arabia levels of differentiation as the gray mangrove at a geographic et al., et al., et al., 2015; et al., et al., et al., suggesting a process of differentiation occurring within the of the Red Sea and the PAG. structure and phylogenetic support the of mangroves within the of the Arabian Peninsula during glacial in long-term geographic and that of the Red Sea as glacial refugia for mangroves et al., as has for marine of the et al., et al., is in the of the PAG, the presence of suitable habitats was during glacial the of the historic to the Sea of the Strait of Hormuz to occur populations from the of the as related to the populations of the Sea of the of the Strait of with of the northern of also a of differentiation in glacial refugia populations in the isolated as the as to a of recent the the northern populations the recent phylogenetic et al., Demographic lineage divergence in (cryptic) glacial of models with to identify the which mangroves from the Red Sea, the and the Arabian Peninsula the Red Sea, revealed that the was consistent with a occurring during a the glacial suggesting that mangroves may the Red Sea the Strait of to the et al., and in the Red Sea are by changes in the and also by periods of and changes in and the results that the levels of and phylogenetic diversity in the Red Sea are the of historical changes in of history such as and geographic also in environmental conditions et al., et al., In the of the PAG, the that revealed a of to to the and the of the the presence of glacial refugia within the by phylogenetic changes in environmental conditions during glacial in of and temperature may to marine glacial periods has for any marine in the PAG. However, conditions of in marine extreme, may suitable for gray which occur in a range of of historic at times of the the of and in with the to are northern and as well as in the Strait of A. marina in a of & & or conditions that of the during glacial of marine glacial refugia for such as and in the northern of the the or the Peninsula et & et al., & 2007; & suggesting that the of local conditions in marine environments during glacial periods may be In to a occurring to the the revealed gene flow between and between the and the Sea of The also detected levels of gene flow between both and suggesting that migration occur as mangrove populations isolated and also the the of the barriers such as the Strait of Hormuz or the marine between and the northern and be as for mangrove as has for species & 2004; et al., with and genetic distance among populations of the northern and suggesting that may and that results may to be for the supported a recent common evolutionary and for the mangroves of The was with a process of diversification occurring the of the driven by geographic isolation and changes in environmental conditions and connectivity resulting from the of the between the populations of the and the Arabian Sea support the of a lineage to the The between the Red Sea by and the Sea lineage at the of the glacial and and at to times the of the Red Sea to the and analyses detected a of gene among and suggesting a of reproductive barriers among upon secondary analyses reveal a process of lineage diversification in the gray mangroves of the Arabian Peninsula that the to glacial for the gray mangrove has at in et al., et al., a that we in analyses as of models was a et al., However, in populations of the to range from to & which that the diversification process may as as as early as in divergence times in systems has with large of & 2018). such as with the in the is to that consistent between models and phylogenetic the for However, the and of phylogenetic and neutral genetic structure in Arabian with the in models, support a diversification process occurring the These divergence within glacial refugia as a in the Arabian mangrove results be in the such as and for results that diversification the the Arabian mangroves system a process of occurring at of to a levels of divergence are at the edge of species’ reduced and habitat can to rapid differentiation to drift in isolation and divergent selection (Lesica & Allendorf, & genetic structure in the of the species distribution to populations of the gray mangrove of the has et al., of speciation in mangrove systems of isolation and gene flow to fluctuations in during glacial periods et al., to may in the of the and the Red analyses reveal multi-loci adaptive divergence driven by environmental extremes In a and a for environmental factors in mangrove related to temperature extremes and and of the in The of by environmental was to the in to in from to et al., et al., et al., & et al., of their to the association the of and revealed adaptive divergence among Red Sea which a of from to in for populations of the the highly divergent association with to the populations of the of the Arabian Sea and These association that local adaptation has a in the differentiation of the mangrove in the Arabian Peninsula for with or the to detected at relevant for adaptation to the extreme and habitats of the seas the Arabian Peninsula. as that in the of within the a in maintaining during conditions & 2012; & 2005). 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In we the Arabian mangroves to analyze the of environmental and neutral in driving and lineage and revealed evolutionary and times of divergence consistent with periods of geographic isolation in glacial refugia both in the Red Sea and the PAG, the of a of was detected as suggesting that geographic distance also an in the differentiation of Arabian mangrove populations. of local adaptation detected among and within the phylogenetic for of the environmental driving adaptive divergence at geographic geographic across the gray mangrove

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