Rapid lineage diversification of gray mangroves ( Avicennia  marina ) driven by isolation in cryptic glacial refugia 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. Summary· Plant 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. Here, we analyzed fully sequenced genomes to study diversification mechanisms in the gray mangroves [Avicennia marina (Forssk.) Vierh.] of Arabia, where they occur at the edge of the species’ range and are subject to variable, often extreme, environmental conditions. · We conducted population structure, phylogenomic and demographic analyses to reconstruct the evolutionary history of the species across Arabia. We also applied genotype-environment association methods to study adaptive mechanisms of lineage diversification. · Our analyses revealed marked genetic structure and highly supported clades among and within the seas surrounding the Arabian Peninsula. Inferred divergence times were consistent with recent periods of low marine connectivity during glacial periods, revealing the presence of (cryptic) glacial refugia in the Red Sea and the Persian/Arabian Gulf. Genetic‐environment association analyses revealed high levels of adaptive differentiation, 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 in plants involves both neutral and selective factors (Rieseberg & Willis, 2007), 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). Evolutionary divergence may result from the accumulation of genetic differences caused by drift in geographic isolation or isolation-by-distance (IBD, Wright, 1943; Wright, 1946), a mode of divergence driven by neutral factors (Mayr, 1954; Mayr, 1963). In turn, geographic variation in environmental conditions can result in divergent selection (Darwin, 1859; Coyne & Orr, 2004), the diversifying process that drives ecological speciation (Nosil, 2012). In ecological speciation models, reproductive barriers arise as a by-product of cumulative, ecologically adaptive changes (Mayr, 1947; Schluter, 2000; Rundle & Nosil, 2005) enabling genome‐wide differentiation at both neutral and selected loci (Nosil et al., 2008; Funk et al., 2011; Shafer & Wolf, 2013; Wang & Bradburd, 2014). Ecological speciation in geographic isolation is theoretically uncontroversial, and considered key in some of the most remarkable radiations in angiosperms (Baldwin & Sanderson, 1998; Hughes & Eastwood, 2006). However, whether environment-driven processes of lineage diversification commonly occur in nature in the absence of long-term isolation and reduced gene flow remains debated in evolution research (Butlin et al., 2008; Fitzpatrick et al., 2008; Papadopulos et al., 2011; 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; Kliber & Eckert, 2005; Crepet & Niklas, 2009).Plant systems occurring in the environmentally heterogeneous and often extreme habitats at species’ range edges 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), frequently 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 the gray mangrove populations of the Arabian Peninsula (Avicennia marina var. marina). The gray mangrove has the broadest distribution of any mangrove species (Spalding et al., 2010; Hogarth, 2015; Tomlinson, 2016), extending across the Indian Ocean and into the West Pacific as far as Japan and New Zealand (Fouda & AI-Muharrami, 1996; Sheppard et al., 2010; Spalding et al., 2010; Khalil, 2015). Gray mangroves present several morphological and physiological adaptations to their harsh intertidal habitat (Tomlinson, 2016), which makes them a compelling model for the study of functional genes and biological pathways involved in selection and stress tolerance in plants (Urashi et al., 2013; Xu et al., 2017). The Arabian Peninsula represents one of the northernmost edges of the species’ distribution (Duke, 1991; Spalding et al., 2010; Tomlinson, 2016), as well as a stressful habitat characterized by extreme temperatures, aridity, and often extreme salinity, factors known to be limiting for mangrove growth (Ball, 1988; Sheppard et al., 1992; Lovelock et al., 2016). Arabian marine domains are also environmentally diverse both within, and among, the main water bodies bordering the peninsula, which define three main biogeographic regions: (i) the Red Sea, where the marine system presents opposing gradients of salinity and temperature, with the highest temperature and lowest salinity in the shallow southern basin, while the deeper northern basin has cooler temperatures but high salinity as a result of limited precipitation and high evaporation (Carvalho et al., 2019; Anton et al., 2020); (ii) the Persian/Arabian Gulf (referred to as ‘PAG’ hereafter) to the northeast of the Arabian Peninsula, where populations are subject to arid (<250 mm) to hyper-arid (<100 mm) rainfall regimes, and experience the widest range of air temperatures in the region throughout the year (Böer, 1997; Whitford & Duval, 2019); and (iii) the Arabian Sea (here including the Sea of Oman), which in contrast with former biogeographic regions, has normal oceanic salinity, and summer temperatures that are buffered by cold-water upwelling as a result of the Indian Ocean monsoon, resulting in more moderate environmental conditions (Claereboudt, 2019).The Arabian Peninsula has experienced large fluctuations in spatial and environmental conditions throughout glacio-eustatic cycles that largely impacted the biodiversity of the region, in particular for the enclosed water bodies of the Red Sea and the PAG (DiBattista et al., 2016a). Throughout the last 400,000 years the Red Sea has remained connected to the Indian Ocean, yet cross-sectional area along the Strait of Bab al Mandab that connects these water bodies was, at times of glacial maxima, as low as 2% of that today, resulting in major increases in salinity and temperature within the Red Sea as well as near-complete isolation at times (Lambeck et al., 2011). For several sustained periods during the last two glacial cycles, the minimum channel width connecting the Red Sea to the Arabian Sea was less than 4 km wide and remained narrow whenever the local sea levels were 50 meters below current levels (Lambeck et al., 2011). In contrast, models show that the PAG was nearly completely drained during the peak of the last glaciation until c.a. 14,000 years ago (Lambeck, 1996). A marine incursion into the southern PAG basin started approximately 12,500 years ago, extending towards the northern basin over the following millennia, with the present day PAG shorelines forming just 6,000 years ago (Lambeck, 1996). In contrast, as an open ocean habitat, the Arabian Sea coast has only experienced vertical migration of sea levels during these glacial periods, without geographic of extreme environmental differential changes in habitat and dynamic barriers to gene flow makes the seas bordering the Arabian Peninsula one of the most marine environments in the with a high for speciation driven by both neutral and selective factors (DiBattista et al., the for of A. marina and species for et al., 1998; et al., 2008; et al., 2016), the gray mangrove populations from the Arabian in analyses et al., 1998; et al., 2000; et al., & The drivers and of local adaptation and lineage diversification in A. marina remain both in and across we the Arabian gray mangrove to extreme habitat conditions and heterogeneous spatial settings genetic at the highly edge of the species’ range and environmental we analyzed of population structure and the evolutionary and demographic history of the species in the Arabian Peninsula. the evolutionary history of the Arabian mangroves were in (i) mangroves from the Red Sea and PAG were during the glacial cycles of the by a the last glacial and (ii) mangroves remained within the enclosed seas in glacial refugia during glacial periods, and sea levels we of adaptive genotype-environment association We environmental and to the and environmental and functional genes involved in local adaptation and lineage and a of marina from across the Arabian Peninsula and one from was from by at and in for to for were was from the to the and with to were and sequenced in a were a for A. marina et al., was with the et al., The resulting of and with a of and a of was and for analyses in structure analyses signs of population structure in Arabian we a of high and neutral of a of and We conducted a as the 2012). We also of population divergence a et al., 2014). We the times with from to among and were with et 2015). of geographic variation in Arabian we for the neutral We genetic with the et al., 2015). geographic were geographic A was and was was the et al., 2015). For we applied the than for population structure yet the population from to be as The and the model were and demographic history model the in et al., to demographic and among mangroves and to the of the isolation in glacial refugia in the enclosed seas Arabia. by the three of models were analyzed for (i) the Red Sea, (ii) the PAG the Sea of and (iii) the Arabian Peninsula. populations were as lineage for of The population was to times of a with the Arabian of years in models et al., et al., 2019; et al., and times of divergence in of models were analyzed of and with and two models were for the Red Sea, the PAG and the Arabian Peninsula, we the from model and are in the & was to model historical of gene flow between mangrove The was the as for the with the of as can be for in the We for in of edges were until of the in between populations was by the model & 2012). The of migration edges was by with 50 for migration edge a from the that the highest are gene with genotype-environment association genotype-environment association to genes environmental and to their to of local adaptation in mangroves from the Arabian Peninsula. We applied a & 1998; et al., as in the et al., 2016). we environmental for the to the and over The of of sea salinity and minimum of sea temperature over from the & as well as and air temperature of the from the et al., 2005; & we population at from a of analyses were a to for genotype-environment between and environmental and a in which in we for population structure for population structure of the two of a the selection. the in et we the analyses to loci involved in divergent selection, between and the of the & and a with the for multiple In to differential association of loci at the we conducted a with the of the as The two were for as well as in the for the populations in the analyses and gene are in the structure and genetic revealed marked levels of population A of the two a of that the geographic distribution of the from the Red Sea and the PAG high within biogeographic along the of the Arabian Sea also marked genetic populations at the and and from the genetic while populations from the Sea of at the and to the The population of a along the The and revealed high levels of differentiation within biogeographic and southern of the PAG along as well as populations from the Arabian Sea, yet to a of the Red Sea along consistent with the populations into two the Red Sea from the Arabian Sea and the The for also revealed the more populations from the of the Arabian Sea and as a with populations along the northeast coast and into the PAG of populations from the northern basin of the PAG and as a populations from northern Red Sea and also as a yet a of with with populations from the Red Sea and and to a In the for populations from the Sea of and with yet levels of with the genetic of the southern PAG basin, which and populations from southern Red Sea and and from the Red Sea yet levels of with the Red Sea population loci revealed a between and genetic among populations marked differentiation between and within biogeographic regions, with populations in clades with high Arabian mangrove populations in three clades or the Red Sea lineage the southern Arabian Sea lineage and the PAG the Sea of lineage the Red the revealed a of consistent with the geographic distribution of the with the northern and and populations and from of the and and populations from Red Sea differentiation and into a The Arabian the populations and occurring in southern which as the of the which Sea of and PAG was into two clades the populations of the northern basin of the PAG and from of the southern basin and and the Sea of and of these two which occur of the Strait of as and demographic history of the Arabian gray models were In the Red Sea, the model with the revealed a for the three analyzed populations an isolation with migration and a to years consistent with a process of lineage among was high from in the Red Sea towards towards the southern For the migration by of and to revealing of these in the In the of the PAG the Sea of the model that also revealed a of in isolation with migration years to the last glacial of some gene flow were detected among PAG than in the Red Sea the also to in most the in the model In the with of biogeographic region of the Arabian Peninsula, the highest to the model including migration and revealed times of years and years with were consistent with the with A model with migration to of the revealing signs of both historical and gene flow among mangrove of migration between the lineage of and the northern populations of both the Red Sea and the PAG highly that these results be with genes and environmental adaptation in Arabian gray of the genetic in the The of the revealed association among biogeographic Red Sea mangroves while the populations with and in the of the Sea of and PAG southern In contrast, the Arabian Sea populations high association with while Red Sea and PAG mangroves association along yet the former with In the environmental the genetic for population structure revealed a more of variation among and within biogeographic regions, where populations from northern PAG high with while populations of the southern PAG and Arabian Sea, as well as from Red Sea, more In the of the highest to with a and to and that and the were to for signs of selection the in et The to of the for an of to of by the In turn, the of the for and from the and were for loci The analyses revealed genetic with one or more of the environmental in both the and the were within of the genes and gene in plants relevant for mangroves in Arabian environment the tolerance to stress et al., by and as well as et al., and water and in to and stress & 2008; et al., 2008; et al., and et al., et al., growth in to stress conditions et al., and stress et al., to salinity stress et al., 2019); tolerance and of species et al., in to stress et al., 2019; et al., differentiation in to et al., et al., and in association with the et al., adaptive is at the we conducted a the of the loci The of the two revealed only by biogeographic from the Red Sea along a air temperature, with northern populations and high Red Sea and to the of and southern Red Sea from the of the Arabian Sea and a with while with a salinity In contrast, populations from the Sea of low association and the of from the PAG an to of the Arabian Sea, also along the yet were and more in the southern basin than in the northern one over populations in the with highest differences among association occurring along the Red Sea and divergence between biogeographic population structure and reveal a process of lineage diversification consistent with isolation in Arabian structure analyses high levels of divergence across Arabia. a and a neutral signs of differentiation, and of genetic that the geographic distribution of mangroves across the seas surrounding the Arabian Peninsula. The analyses also marked genetic differentiation between the populations from the the and the of the basin of the Red as well as between the northern and southern of the levels of between the populations of the southern PAG basin and the Sea of were also lineage or gene flow between We also a between neutral genetic differentiation and geographic among that may for a large of the population structure in the and revealed a of among Arabian mangrove and occurring in the Red Sea, the Arabian Sea and the with the including the populations of the Sea of of divergence among Arabian biogeographic for marine et al., 2015; et al., et al., et al., et al., with the geographic distribution of the species and with barriers to gene flow (DiBattista et al., et al., However, marine in levels of differentiation at such geographic as the gray a process of population differentiation occurring within the enclosed water bodies of the Red Sea and the population structure and support the of mangroves within the enclosed water bodies of the Arabian Peninsula during glacial cycles, where in long-term geographic and that of the Red Sea basin as glacial refugia for mangroves (Lambeck et al., as has for marine of the region (DiBattista et al., et al., is in the of the where the presence of suitable habitats was limited during glacial periods, where only the of the to the Sea of the Strait of to occur (Lambeck, 1996). populations from the southern basin of the PAG as more related to the populations of the Sea of the of the Strait of than with of the northern PAG of also a of differentiation in glacial refugia where populations in the isolated as the as to a of recent throughout the PAG the where northern populations the most recent et al., lineage divergence in (cryptic) glacial refugia by gene flow of demographic models were with to the most which mangroves from the Red Sea, the PAG and the Arabian Peninsula For the Red Sea, revealed that the most was consistent with a occurring during a the three last glacial cycles, that mangroves may the Red Sea basin the Strait of Bab to the Indian Ocean 400,000 years ago (Lambeck et al., and cycles in the Red Sea are characterized by changes in the sea and but also by periods of and changes in salinity and the results that the levels of population and in the Red Sea are the of historical changes in of population history such as and geographic but also in environmental conditions (DiBattista et al., et al., In the of the the model that revealed a of to nearly years ago, to the and the of the enclosed Inferred the presence of glacial refugia within the changes in environmental conditions during glacial maxima, in of salinity and temperature may physiological to marine glacial periods has for any marine in the However, conditions of intertidal in marine while extreme, may remained suitable for gray which occur in a wide range of of shorelines at times of the show the of and in several with the main to are northern and southern as well as in the Strait of A. marina in a of et al., & or conditions that of the PAG during glacial of marine glacial refugia for such as and in the northern area of the the or the Peninsula et et al., 2005; et al., et al., et al., that the of local conditions in marine environments during glacial periods may be In to a occurring to the the demographic model revealed gene flow between PAG and between the southern basin and the Sea of The also detected levels of gene flow between both and that some migration occur as mangrove populations isolated and also the the of the PAG barriers such as the narrow Strait of or the marine between and the northern and southern basin be as limiting for mangrove as has for species et al., et al., highest model for the Arabian Peninsula revealed times of divergence among major with a process of diversification occurring over the biogeographic of the peninsula, driven by geographic isolation and changes in environmental conditions and connectivity resulting from the glacio-eustatic cycles of the between the populations of the PAG 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 last glacial and and at to times the of the Red Sea to the Indian and analyses detected a of gene among and a of reproductive barriers among analyses reveal a process of lineage diversification in the mangroves of the Arabian Peninsula the last two to three glacial results that the the Arabian mangroves system represents a process of occurring at of to a for the gray mangrove has at years in et al., 2019; et al., of demographic models was a et al., 2016), and we in However, in populations of the PAG to range from to years et al., which that the diversification process may to as as to 6,000 or levels of population divergence are at the edge of species’ where reduced population and habitat can to rapid differentiation to drift in isolation and divergent selection (Lesica & Allendorf, & 1996). genetic structure in the of the species distribution to populations of the gray mangrove of the West Pacific has et al., 2006). of speciation in mangrove systems cycles of isolation and gene flow to fluctuations in sea during glacial periods et al., to may in the enclosed water bodies of the PAG and the Red analyses reveal multi-loci adaptive divergence driven by environmental a and a for population structure, key environmental for mangrove and of the in population The of by environmental was to the in to genotype-environment in from to et al., et al., 2019; et al., et al., et al., We also genes with one or more the to detected at relevant for adaptation to the extreme and habitats of the seas the Arabian Peninsula. These mechanisms to with such as temperature salinity or and or the and over revealed adaptive divergence among Red Sea which along a of temperatures from to The Red Sea present major differences along the strong results in air and sea temperatures the and yet minimum temperatures In contrast, salinity increases to limited precipitation and high and minimum air temperatures below with a in and et al., et al., a several the and southern of the Red Sea to be et al., 1992; et al., 2019; & in for populations of the PAG were less yet the highly divergent association with to the populations of the of the Arabian Sea, along salinity and is with the environmental conditions in the with air temperatures the from to the year in (Böer, 1997; Whitford & Duval, resulting in low history and environmental selection rapid lineage diversification in the gray mangroves of diversification processes in plants are with large fluctuations in habitat and connectivity (Rieseberg & Willis, In we the Arabian mangroves to the of spatial environmental and neutral evolution in driving population and lineage and demographic revealed evolutionary and times of population divergence consistent with periods of geographic isolation in glacial refugia both in the Red Sea and the the of a A of was also that geographic may also an in the differentiation of the times were providing of a rapid process of diversification within the enclosed Red Sea and PAG water bodies during the of differential local were among for of the biogeographic regions, and also among the populations within the Red Sea, revealing divergent ecological within biogeographic selection among PAG and Sea of populations may than in the Red Sea as a result of more limited environmental and during periods, as populations to more from the less extreme environment of the Arabian Sea also of a process of adaptive differentiation among the main mangrove of the Arabian Peninsula. the results in study support a process of rapid diversification driven by the combined factors of environmental selection and historical events, and reveal mangrove peripheral populations of as for lineage diversification and of evolutionary in to environmental are to for and We and for their in the We the Abu and the of and of for providing for research related to was supported by New York University Abu by and University of and to and evolutionary and with of the Arabian mangrove populations in study and The of analyzed for is in Red Sea Arabian Sea & Sea of Persian/Arabian Gulf

Fetched live from OpenAlex and de-inverted. Abstracts are not stored in this database: the inverted indexes are 8.6 GB of the frame’s 9.3 GB of text, and the host has 13 GB free.