Island biogeography of the megadiverse plant family Asteraceae

Domain: earth_science
Published: 2024-08-23
Editorial outcome: minor_revision

Abstract
The megadiverse plant family Asteraceae forms an iconic component of island floras including many spectacular radiations, but a global picture of its insular diversity is lacking. Here, we uncover the global biogeographical and evolutionary patterns of Asteraceae on islands to reveal the magnitude and potential causes of their evolutionary success. We compile a global checklist of Asteraceae species native and endemic to islands and combine it with macroecological analyses and a phylogenetic review of island radiations. Asteraceae have a global distribution on islands, comprising approximately 6,000 native island species, with 58% endemics. While diversity of the family on islands is lower than expected given its overall diversity, Asteraceae are the most diverse family on oceanic islands, suggesting an exceptional ability to thrive in isolation. In agreement with island biogeography predictions, native Asteraceae diversity increases with area and decreases with isolation, while endemism increases with both. We identify 39 confirmed island radiations and 69 putative radiations, exceeding numbers for other iconic insular groups. Our results reveal Asteraceae offer immense potential for research in ecology and evolution, given their close tracking of island biogeography expectations, large number of both species and radiations, cosmopolitan distribution, and numerous undiscovered radiations.

Introduction
The top ten most diverse plant families make up 43% of angiosperm species1. Understanding the distribution and drivers of diversity of these large families is thus a crucial step toward explaining the success of flowering plants in general. Key biogeographical settings for exploring the patterns and processes that shape angiosperm diversity are islands. Due to their distinct boundaries, global distribution, and replication, island systems have played a crucial role in the development of key evolutionary and ecological theories2–8. The geographic isolation and unique habitats found on islands have given rise to remarkable angiosperm biodiversity that is often characterized by high levels of endemism9,10, adaptive radiations11,12, paleoendemism13,14, and repeated evolution of convergent traits15,16.

While islands are valuable natural laboratories for studying plant diversity, global-scaled data on the distribution of major plant families on islands are only starting to emerge. Recent global studies have explored biodiversity patterns for a few major families and lineages on islands17,18, factors impacting the assembly of island floras19–22, and traits associated with insular diversity23–26. These studies reveal how links between island features (e.g., area, isolation, age, and climate), functional traits (e.g., insular woodiness), and biogeographical rates (e.g., colonization, speciation, and extinction) are important determinants of the number of native and endemic species of flowering plants on islands, whilst suggesting that evolutionary success on islands may not necessarily mirror that found on continents27.

Out of all plant families, arguably the one most often associated with evolutionary success on islands is the most diverse family of all—Asteraceae. Commonly known as the daisy or sunflower family, Asteraceae (Compositae) boasts the greatest species number of any plant family in the world, with an estimated 32,000–34,000 species1,28,29. Species of this family are native to every continent except Antarctica and are found in a wide range of habitats, but are most abundant in dry and semi-arid habitats and in Mediterranean-type ecosystems, deserts, grasslands, and mountains30. Members of the family show great variation in growth habits and range from small annual herbs to woody perennial shrubs, lianas, and trees. Additionally, some species exhibit specialized habits such as cushion forms, succulents, and even, in rare cases, are epiphytic and aquatic plants.

On islands, Asteraceae are thought to be remarkably diverse, and often form an iconic component of insular floras of both continental and oceanic origin. For instance, it is the most species-rich family on the remote Juan Fernández Archipelago31 with 30 native species and four genera endemic to the islands, and is among the top five most diverse families on the large continental island of Madagascar32. Additionally, the family has high levels of endemism on oceanic islands: a study by Lenzner et al.33 compiled diversity data on major plant families across 14 oceanic archipelagos and found that Asteraceae had the highest number of single-island endemics for the oceanic islands considered in the study. Their success in dispersal, establishment, and diversification on islands has been suggested to result from a combination of intrinsic factors3,34,35: Asteraceae possess unique fruit morphology that aids in long-distance dispersal36,37; their head-like inflorescence (capitulum) often attracts generalist pollinators; and they are capable of several breeding systems that may favor establishment on islands. Many island species are self-compatible23, while species in several island lineages are functionally self-incompatible with the capacity to self-seed and a genetic system (i.e., sporophytic self-incompatibility) that aids both in the establishment of small populations and the retention of genetic diversity after arrival38.

In addition to a high native and endemic species richness on islands, Asteraceae are known for their presumed propensity to radiate (that is, to undergo cladogenesis in situ on islands at relatively fast rates). Two recent studies, one reviewing adaptive radiations across flowering plants39 and another focused on adaptive radiations on oceanic islands across all taxonomic groups40, both found Asteraceae to be overrepresented in terms of adaptive radiations compared to other clades. Indeed, the family provides numerous examples of spectacular island radiations: Scalesia on the Galápagos Islands41, the woody Sonchus alliance on the Canary Islands42, Dendroseris on the Juan Fernández Islands43,44. One of the textbook examples of adaptive radiation on islands is the Asteraceae silversword alliance of Hawai‘i, a clade of 33 species in three endemic genera (Argyroxiphium, Dubautia, Wilkesia), which evolved from a common ancestor that colonized Hawai‘i by a long-distance dispersal event from North America around 5 million years ago (Mya), and which exhibit high diversity in morphology and ecological adaptation45–47. Another notable example is the Hawaiian Bidens. The monophyletic 20 species of Bidens endemic to Hawai‘i originated from a single colonization event c. 1.8 Mya, having thereafter radiated across the archipelago, occupying a wide variety of different habitats including sand dunes, lava fields, rainforests, and wetland bogs, and have the highest rates of speciation per unit area documented for any island plant radiation to date48,49.

An increasing number of phylogenetic studies focusing on selected island clades of Asteraceae from specific islands or archipelagos41,47,50–52 are providing insight into the potential drivers of diversification in those Asteraceae groups. One hypothesis is that the high diversity of Asteraceae on islands results from a combination of high continental diversity, high rates of long-distance dispersal, and overall high rates of in situ speciation that well exceed extinction rates (consistent with the high net diversification rates observed in continental Asteraceae)53–56.

While it is assumed from the above examples that Asteraceae are highly diverse on islands and have a propensity to radiate, in fact, a complete global picture of the diversity and distribution of the family is yet to be assembled. Furthermore, an assessment of Asteraceae’s potential to radiate across islands globally is still lacking, because previous studies focused solely on confirmed adaptive radiations and/or on oceanic islands, and thus the magnitude of island radiations within the family is unknown.

In this work, we compile a global checklist of island Asteraceae and use this to answer four key questions: (1) How does the island species richness of Asteraceae compare with that of other flowering plant families? (2) How is island Asteraceae diversity distributed across space and major clades of the family? (3) What are the environmental and biogeographical drivers of native and endemic insular diversity on islands? (4) How many island radiations have occurred within Asteraceae and are there commonalities between radiations? We show that Asteraceae have a truly global distribution on islands, with 6135 native island species, 58% of which are endemic. Our findings reveal that while the diversity of the family on islands is lower than expected given their overall diversity, Asteraceae are the most diverse family on oceanic islands, suggesting an exceptional ability to thrive in isolation. Moreover, diversity patterns in Asteraceae follow classic island biogeography theory, with area and isolation being the strongest predictors of species richness and endemism, and the numerous confirmed and understudied radiations highlight the family’s potential as an ideal study system in ecology and evolution.

Results
Asteraceae are one of the most diverse families on islands
Among angiosperms, Asteraceae are the largest family in the world with 32,000–34,000 species globally. Our comprehensive checklist of insular Asteraceae shows that this family is also remarkably diverse on islands: we found 6135 species of Asteraceae are native to islands, of which 3535 (58%) are endemic to islands globally. On oceanic islands specifically, we found 1833 native Asteraceae species and 955 (52%) endemic species.

As Asteraceae species are generally perceived to be good dispersers and excellent island colonizers3,36, the proportion of island native and endemic species of the total Asteraceae species pool would be expected to be higher in Asteraceae than in other large families, and higher than expected by chance. Surprisingly, our comparison between the diversity of angiosperm families on islands showed that Asteraceae are not the most species-rich family across all islands (Fig. 1 and Supplementary Table 2) and that they are underrepresented in terms of island species given its overall diversity (Fig. 1 and Supplementary Table 3). These results align with a recent study focused on island disharmony in plants22, which found that while Asteraceae are generally underrepresented on islands given their species richness in mainland source pools, the family is nonetheless pervasive on islands. Orchidaceae and Rubiaceae have the highest number of native island species with 11,188 and 6188 species respectively. The high insular diversity of Orchidaceae and Rubiaceae is found disproportionately on large, tropical continental islands and archipelagos (including New Guinea, Borneo, and the Philippines), which are not particularly rich in Asteraceae species. On oceanic islands, Asteraceae are the most diverse family for both the number of native and endemic species. Yet, despite high species richness compared to other families, Asteraceae diversity on oceanic islands is lower than expected given their diversity globally (Fig. 1B).

Island species account for 18% of the total species diversity of Asteraceae (Supplementary Table 2). Using a binomial test we found that the observed number of Asteraceae species native to islands is significantly different than expected based on the proportion of Asteraceae to angiosperms globally (10%) and that the island proportion (6%) is significantly lower than expected under a null model (Supplementary Table 3 and Fig. 1). Additionally, a comparison of the observed number of island Asteraceae species to the island community simulations confirms that the observed number of island species is lower than the null expectation across all islands and oceanic islands (Fig. 1).

Clade age could be a factor contributing to the differences in island diversity between plant families. The diversity of the mainland species pool of each family is influenced by family age and global diversification rates. Notably, among the ten most diverse families on islands, Asteraceae are the youngest family (Supplementary Table 2), which could account for their underrepresentation on islands, as younger families may have been less diverse with smaller mainland pools at the time of emergence of the islands in our dataset, thus giving them a colonization “disadvantage” earlier on. However, most of the islands in our dataset are much younger than the age of the families (Supplementary Fig. 1) suggesting that the primary biogeographic causes of the underrepresentation on islands are to be found in lower colonization and/or diversification rates since island origin. As more phylogenetic data of island species becomes available, models of island biogeography, such as the Dynamic Assembly of Islands through Speciation, Immigration and Extinction (DAISIE) model57,58, can be used to estimate rates of colonization, speciation, and extinction for entire island communities of each family over evolutionary timescales.

Asteraceae have a global distribution across islands
Native species of Asteraceae have a truly global distribution across the world’s islands (Fig. 2). In our global checklists, Asteraceae occur natively on 791 islands including 308 oceanic islands, and across 146 archipelagos. Their distribution reaches north to the Svalbard Islands and Greenland (80°N and 75°N) and south to Macquarie Island and Heard Island (55°S and 53°S). Insular diversity ranged from one (minimum inclusion criterion) to 550 native species, with 29 islands (4%) harboring more than 100 native species and 155 islands (20%) harboring only one native species (our dataset only includes islands with at least one native Asteraceae species). Across all island types, 128 islands (16%) have at least one endemic species.

While its distribution is global, the diversity of the family is not evenly distributed geographically, and several island regions are notable hotspots of diversity. Madagascar is the most diverse island overall for both native (550) and endemic (487) species. The Caribbean, in particular the Greater Antilles with 671 native and 430 endemic species, is another major center of island Asteraceae diversity. At the island level, three large islands (Cuba, Hispaniola, Jamaica) are all in the top ten most diverse islands globally for number of endemic species (196, 145, and 58). This pattern of the Caribbean as an important area of endemism for the family furthers supports a review by ref. 59, who found that the region has the highest number of endemic genera in Asteraceae globally. Across oceanic islands, Macaronesia, the Hawaiian Islands, and the Mascarenes are hotspots of island diversity. The Canary Islands is the most diverse oceanic archipelago with 299 native species, and seven of the ten most diverse oceanic islands for native species are islands in the Canaries, with Tenerife being the most species-rich (159 species). The Hawaiian Islands are the second most diverse oceanic archipelago with 102 native and 95 endemic species, and have a remarkably high proportion of endemism (93%), followed by the Mascarenes with 79 native and 64 endemic species.

In comparing hotspot regions, the British Isles (850 native species and 368 endemic species) and Iceland (334 native species and 261 endemic species) stand out as diversity anomalies. While these two regions appear as hotspots of island diversity, the majority of species in these two island regions are apomictic60. Apomixis, a mode of asexual reproduction in which seeds are produced without fertilization, is a poorly understood trait in Asteraceae61 and one that challenges taxonomic species concepts and delimitation62. To investigate the impact of apomictic species on our results, we performed a sensitivity analysis with apomictic genera removed (see Supplementary Fig. 5), which revealed minor changes to the ranking of top island hotspots, but no effect on our findings otherwise (including the models).

The diversity of island species is also unevenly distributed across the major clades and taxonomic tribes of the family (Fig. 3). The tribe with the highest number of native island species is Cichorieae (1660 spp.); while this tribe is an important component of island floras (e.g., Tolpis and the woody Sonchus alliance in Macaronesia, Dendroseris in the Juan Fernández Islands), its overall diversity is inflated due to the high number of apomictic species, well-known in this tribe (e.g., Hieracium on Iceland, Taraxacum on the British Isles).

Aside from Cichorieae, the three most diverse tribes for both native and endemic island species are Astereae (793 native island species, 465 endemic species), Senecioneae (653, 447), and Gnaphalieae (589, 339). Together, these four widespread tribes make up nearly 60% of all native insular Asteraceae species (Supplementary Table 4 and Supplementary Fig. 3). While these tribes are also some of the largest tribes in the family, when we compare observed island diversity to expected diversity given the overall size of the tribe (Supplementary Table 5), we find that island species are overrepresented in Cichorieae, Astereae, and Gnaphalieae and within the expected range for Senecioneae. The two tribes with the highest proportion of native island species compared to the total diversity are Feddeeae (100%) and Distephaneae (86%). Feddeeae is a monotypic tribe with a single species, Feddea cubensis endemic to Cuba (Supplementary Fig. 3). The Distephanus clade is a group distributed across Africa, Madagascar, and the

Methods

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "In their paper \"Asteraceae in isolation: Diversity and island biogeography of the largest plant family,\" Roeble et al. examine the diversity of Asteraceae on islands. This study is important, as at least two groups of Asteraceae are adaptive radiations across archipelagos and representatives of the family make up a large percentage of insular taxa. To assess species diversity, the authors amassed and curated a large collection of species occurrence data and their distributions on islands and discovered that the group is actually a bit scarcer on islands given the total amount of diversity, but that some notable taxonomic groups exist that should be studied as representatives of island radiations.\nI will begin my review with an overview of broader issues, followed by minor issues.\nOn line 111, the authors list the questions they will answer, which includes question #3: What are the environmental and biogeographical drivers of native and endemic insular diversity on islands? I do not believe that this question was answered directly.\nI see it as important that within families the authors compared the island species to those that occur on continents. However, there is a problem in comparing across families. The expected species on islands would be determined by the clade age as well as its diversification rate. The latter point would be difficult to estimate and one could assume that all families diversified at nearly the same rate (yes, this is probably violated), but we have the data to address the former point. Ignoring clade age makes the assumption that all families evolved at the same time; this most certainly is untrue.\nThe most diverse tribes on islands were the Cichorieae, Astereae, Senecioneae, and Gnaphalieae. Aside from the Astereae, the remaining three tribes are notoriously weedy. I was surprised that the invasiveness of those tribes was not considered in the context of this work as the ability of these tribes to colonize novel areas and establish in them is likely to be much greater than just their ability to colonize islands. Further, I was surprised to not see the Cardueae listed, as they are also known as being weedy. I would expect to see them overrepresented on islands, but they are not according to the analyses. Perhaps this is due to the use of taxonomic categories rather than a phylogenetic approach, as they are well represented on islands (see Table S5).\nIn Figure 4 (which I enjoyed), why was Temperature seasonality used for NSR and Annual temperature used in pSIE? Also, why not show the individual results for pSIE and Max elevation and Annual temperature, as was done for the other measures?\nI wish that I saw a stronger argument that the composites were doing something exception on islands compared to what they are doing on continents. But at the end of this study, they are less diverse on islands than on continents. Perhaps the most interesting thing that is occurring is the change in morphological forms on islands (e.g., silversword alliance) as they become woody. I agree with the authors that this study does illuminate several groups that warrant additional studies, but overall it doesn't seem like islands are important determinants of species diversity in the family.\nThe results presented in Figure 5C were interesting, but I would have liked to see a statistical analysis conducted to determine whether those values were greater or less than what we would expect by chance. Furthermore, it was really difficult to read the key.\nMinor comments:\nLine 29: I think Carlquist's Island Biogeography should be cited here, it was incredibly important work.\nLine 56: I would also include cushion forms.\nLine 153: Could you please explain better what the trait \"botanical continent\" means?\nLine 249: What was the threshold used in the VIF analysis?\nLine 527: I think greater care must be taken when comparing Asteraceae to other groups, like birds. There are over twice as many composites as birds and by chance we should expect there to be more cases of island radiations.", "reviewer_2": "The paper by Roeble et al. looks into the diversity of Asteraceae in islands. I really enjoyed reading this manuscript, I think it is very well written and the methods are comprehensive. To my knowledge, this is the first study that looks into the insular diversity of this mega-diverse family on a global scale. The results show that despite Asteraceae being the most species rich family of plants, it is not the most specious on islands. It also shows how species richness increases with area of the island but decreases with isolation, whereas number of single-island endemics increase with both area and isolation.\nI only have a couple of small comments.\nResults and Discussion, line 334. “Asteraceae are also underrepresented on oceanic islands given their overall diversity”. The meaning of this was not clear to me. Do you mean not well sampled, identified, or understudied?\nLine 522. “How the overall number of island radiations within Asteraceae compares to other flowering plant families still remains unknown”. I thought that is what you did in this study. Isn’t one of the questions of this paper “How does the island diversity of Asteraceae compare with that of other families?”. Please clarify.\nIn the methods, it is mentioned that you looked into “traits often hypothesized to be associated with island radiations (breeding system, dispersal syndrome, ploidy level, hybridization)” (lines 303-305). However, in the discussion there is no mention about your findings on ploidy or hybridization patterns. Did you find anything there worth mentioning? Hybridization is often seen as one of the drivers of genetic diversity in several insular plant groups, so I’m wondering if it could play a role in Asteraceae as well?", "reviewer_3": "This manuscript represents a comprehensive and careful, analytical synthesis of patterns and correlates of island diversity and diversification in the most diverse family of flowering plants, Asteraceae. The results advance understanding of island biogeography significantly by revealing unexpected hotspots of diversity within a global perspective and demonstrating that this family of plants, which is often regarded as exceptional and therefore possibly unhelpful for explaining broader-scale biogeographic phenomena, in fact conforms to expected biogeographic rules and is therefore an excellent subject for studying biogeographic phenomena in general (as concluded by the authors). Equally importantly, the study serves to highlight a large diversity of genera worldwide that are understudied and warrant close attention as putative radiations that may hold important secrets for island biology. Perhaps most of all, this study has generated a significant diversity of resources, such as global lists and traits of island composites, that will serve researchers going forward and will ensure that it is a go-to reference for future investigations, thus magnifying its impact and citation. I enthusiastically recommend its publication.\nMinor suggestions/corrections:\nLine 43: “biogeographical rates” is perhaps a bit unclear as to what is being included here.\nLine 52--53: There are two naturalized species of Asteraceae now known from Antarctica, so probably best to change “occur on” to “are native to” here.\nLine 70: In addition to capacity for selfing, it may be worth noting that self-incompatible island composites (including representatives of some of the more diverse island radiations, such as taxa of Dendroseris, Scalesia, etc.) have sporophytic SI, where dominance relationships among S-alleles may allow for some degree of selfing and inbreeding more generally, which may facilitate both establishment after dispersal and retention of genetic diversity under insular conditions, favoring adaptation (Crawford et al. 2009, already in the references, could be cited for this point, but especially see a just-released review of reproductive biology in oceanic-island Asteraceae by Crawford et al. 2024 Bot Rev). The authors note later in the manuscript that data are still sparse on breeding systems across the family, and that point is very well taken.\nLines 325-327: The finding of lower-than-expected species diversity of Asteraceae on islands based on overall species diversity in the family was also concluded by a recent analysis of island disharmony (König et al. 2021) that is already in the references and could be cited here.\nFig. 3: The position of Abrotanella shown here is accidentally indicated by an arrow and in the caption as belonging to tribe Astereae, rather than to tribe Senecioneae, where all evidence places it (and where it is indicated as belonging in the supplementary data).\nTable S4: The column headings “Subfamily” and “Tribe” are reversed here.", "reviewer_4": "This is an impressive contribution towards the understanding of plant diversity on islands and specially of mega diverse Compositae.\nThe text reads very well and the excellent figures complement brilliantly the thorough compilation of information and results presented in the article. This is a contribution worthy of publication. My comments are only minor and are detailed as follows.\nPage 2, lines 49-50\nWhen providing aka names, Compositae should appear first. Notice that this is a standard scientific name, not the common name used on line 50 as “composite”\nPage 3, line 74.\nThe sentence start alluding to two studies, but only one is cited. I understand authors refers also to the one mentioned in line 75… but it is a bit confusing nonetheless.\nPage 3, line 77\nPerhaps it is an editorial policy behind the lack of authors on scientific names, but these names MUST have authority the first time they appear on text.\nPage 7, line 289\nCheck citation syntax\nPage 12, Figure 3\nPlant drawing # 3 with some minor re-arrangements of #1 and #2 could be conveniently placed next to the Senecioneae bar\nPage 16, line 512\nReplace “6” with six. Please check throughout text as there are several other instances that need such replacements."}, "author_response": "Response to Reviewers’ Comments\nReviewer #1\nIn their paper \"Asteraceae in isolation: Diversity and island biogeography of the largest plant\nfamily,\" Roeble et al. examine the diversity of Asteraceae on islands. This study is important,\nas at least two groups of Asteraceae are adaptive radiations across archipelagos and\nrepresentatives of the family make up a large percentage of insular taxa. To assess species\ndiversity, the authors amassed and curated a large collection of species occurrence data and\ntheir distributions on islands and discovered that the group is actually a bit scarcer on islands\ngiven the total amount of diversity, but that some notable taxonomic groups exist that should\nbe studied as representatives of island radiations.\n● Thank you for the positive assessment. We have addressed all your thoughtful\ncomments below.\nI will begin my review with an overview of broader issues, followed by minor issues.\nOn line 111, the authors list the questions they will answer, which includes question #3: What\nare the environmental and biogeographical drivers of native and endemic insular diversity on\nislands? I do not believe that this question was answered directly.\n● In our study, we use analytical and statistical tools from macroecology to explicitly\ninvestigate the main potential drivers of island diversity in the family Asteraceae.\nThus, we aimed to answer this question directly through a mixed-effects modeling\napproach that tested a range of potential biogeographic and environmental variables\ncorrelated with diversity, and we think we have successfully achieved this goal by\nidentifying island area, isolation and island types as major drivers of insular\nAsteraceae diversity (see Results and Discussion section ‘Drivers of island species\nrichness and proportion endemism’). However, we do acknowledge that\nmacroecological analyses can reveal associations between explanatory variables\n(“drivers”) and response variables that do not necessarily indicate causation. Our\npreference though is to keep the word “drivers”, as this is standard terminology in the\nfield, but this word could also be replaced by “correlates”.\nI see it as important that within families the authors compared the island species to those\nthat occur on continents. However, there is a problem in comparing across families. The\nexpected species on islands would be determined by the clade age as well as its\ndiversification rate. The latter point would be difficult to estimate and one could assume that\nall families diversified at nearly the same rate (yes, this is probably violated), but we have the\ndata to address the former point. Ignoring clade age makes the assumption that all families\nevolved at the same time; this most certainly is untrue.\n● Thank you for raising this important consideration. We have now included family age\nin our comparison of differences in insular diversity among plant families. We\nextracted the stem age for each family with native species on islands from\nRamírez-Barahona et al., 2020, a recent study that constructed and dated a\ncomplete family-level angiosperm phylogeny consisting of all 435 currently\nrecognized families and calibrated with 238 fossils. Note: we opted for the stem age\nestimates in the Ramírez-Barahona et al., 2020 phylogeny due to their extensive\ncalibration points, over the recent Zuntini et al., 2024 Nature angiosperm phylogeny.\nWe expanded our approach to (1) compare the stem age of the families with native\ninsular species to the ages of the islands (see new Figure S1) and (2) compare the\nstem ages of the top ten most diverse families on islands (see updated Table S2).\nWith this, we then expanded our discussion to also include family age as a potential\nfactor.\n● (Lines 141-153) “Clade age could be a factor contributing to the differences in island\ndiversity between plant families. The diversity of the mainland species pool of each\nfamily is influenced by family age and global diversification rates. Notably, among the\nten most diverse families on islands, Asteraceae are the youngest family (Table S2),\nwhich could account for their under-representation on islands, as younger families\nmay have been less diverse with smaller mainland pools at the time of emergence of\nthe islands in our dataset, thus giving them a colonization “disadvantage” earlier on.\nHowever, most of the islands in our dataset are much younger than the age of the\nfamilies (Figure S1) suggesting that the primary biogeographic causes of the\nunderrepresentation on islands are to be found in lower colonization and/or\ndiversification rates since island origin. As more phylogenetic data of island species\nbecomes available, models of island biogeography, such as the Dynamic Assembly\nof Islands through Speciation, Immigration and Extinction (DAISIE) model (Valente et\nal., 2015; Valente et al., 2020), can be used to estimate rates of colonization,\nspeciation, and extinction for entire island communities of each family over\nevolutionary timescales.”\nThe most diverse tribes on islands were the Cichorieae, Astereae, Senecioneae, and\nGnaphalieae. Aside from the Astereae, the remaining three tribes are notoriously weedy. I\nwas surprised that the invasiveness of those tribes was not considered in the context of this\nwork as the ability of these tribes to colonize novel areas and establish in them is likely to be\nmuch greater than just their ability to colonize islands. Further, I was surprised to not see the\nCardueae listed, as they are also known as being weedy. I would expect to see them\noverrepresented on islands, but they are not according to the analyses. Perhaps this is due\nto the use of taxonomic categories rather than a phylogenetic approach, as they are well\nrepresented on islands (see Table S5).\n● We agree that weediness is an interesting topic in the context of insular plants, and\nthis is a good topic for future studies. We explicitly limited our study to species native\nto islands in order to focus on the natural processes shaping diversity on islands. To\nfurther clarify this we added the following to the Methods Data Collection: “Species\nnon-native or introduced to each island were excluded”. While analyzing\ninvasive/introduced/alien species is out of the scope of this paper, we agree that\nweediness is an interesting aspect and we have now expanded the discussion to\ninclude your recommendation on this complex of trait.\n● (Lines 212-216) “Additionally, several tribes with high island species richness, such\nas Gnaphalieae and Senecioneae, are well-known for having widespread “weedy”\nspecies characterized by a combination of traits that promote colonization, fast\ngrowth, and dominance. Future research on the widespread weedy species that\noccur natively on islands could provide insight into traits that facilitate successful\ncolonization and establishment in novel habitats on islands.”\n● Regarding Cardueae: for native island species this is indeed an important tribe,\nexhibiting the fifth highest overall diversity. Yet, despite their overall diversity,\nCardueae are under-represented on islands for native species richness given the\noverall number of species in the tribe (Table S5). We focused the presentation of the\nresults in the main text on the bigger picture patterns to fit with the general\nreadership of Nature Communications; however, the individual results for each of the\ntribes are visualized in the main text Figure 3 and detailed in the Supplementary\nTables S4 and S5.\nIn Figure 4 (which I enjoyed), why was Temperature seasonality used for NSR and Annual\ntemperature used in pSIE? Also, why not show the individual results for pSIE and Max\nelevation and Annual temperature, as was done for the other measures?\n● We carried out model selection (described in detail in the methods and Table S1) for\nboth NSR and pSIE independently to identify the best supported global model for\neach. Based on model selection, temperature seasonality is the best climatic\npredictor for NSR, while mean annual temperature is the best climatic predictor for\npSIE (described in the results, lines 239-241). We have updated the text in the\nmethods to make this clearer.\n● (Lines 498-502) “We employed AIC-based model selection independently for the (1)\nNSR and (2) pSIE models, choosing the best supported global model for each from a\nset of candidate models (19 for NSR and 15 for pSIE) (see Table S1). The models for\nNSR and pSIE are independent, with potentially different environmental variables\nexplaining variation in each of the two measurements of diversity best.”\n● In the initial version of Figure 4B, only significant variables were plotted. We have\nnow updated Figure 4B to plot all the individual variables.\nI wish that I saw a stronger argument that the composites were doing something exception\non islands compared to what they are doing on continents. But at the end of this study, they\nare less diverse on islands than on continents. Perhaps the most interesting thing that is\noccurring is the change in morphological forms on islands (e.g., silversword alliance) as they\nbecome woody. I agree with the authors that this study does illuminate several groups that\nwarrant additional studies, but overall it doesn't seem like islands are important determinants\nof species diversity in the family.\n● Our study is the first comprehensive data-driven review of Asteraceae on islands,\nand our results challenge previous assumptions (based on research around single\nlineages or a subset of island types) that Asteraceae are exceptional on islands. We\nare convinced this is a key and novel result: while Asteraceae are not exceptionally\ndiverse on islands compared to their overall diversity, in fact, the family remains an\nexcellent model for exploring broader-scale biogeography patterns on islands\nbecause they conform to expected island biogeography rules while offering a large\nsample size (occurring on many islands worldwide with a large number of species).\nThis point is emphasized in the conclusion.\n● We also agree that trait evolution in insular Asteraceae is an important and\ninteresting topic for continued research. To this end, we reviewed traits associated\nwith island radiations and identified understudied traits (data deficient). Woodiness is\nindeed well represented in insular Asteraceae throughout the world (e.g. Scalesia in\nthe Galapagos, Sonchus in the Canary Islands). Nevertheless, this character is also\nfound in other insular families: Echium (Canary Islands), Viola and Geranium\n(Hawai´i), etc. (see Zizka et al., 2022 PNAS). We are confident our comprehensive\nreview of island radiations in Asteraceae, both confirmed and putative, provides a\nuseful guide for future research on groups and traits that warrant closer attention.\n● We respectfully disagree that islands are not important in explaining the diversity\npatterns of Asteraceae: as we highlight throughout the manuscript, islands harbor c.\n6,000 native species, they are key locations for narrowly distributed endemics,\nsuccessful long-distance dispersal events, evolution of novel forms, and support a\nhigh number of radiations.\nThe results presented in Figure 5C were interesting, but I would have liked to see a\nstatistical analysis conducted to determine whether those values were greater or less than\nwhat we would expect by chance. Furthermore, it was really difficult to read the key.\n● Thank you for this suggestion. We have now expanded the discussion to include a\ncomparison of our results with traits associated with speciation observed in other\nplant families on islands (lines 351-367). A statistical analysis to determine whether\nisland trait values are greater or less than expected would require complete trait\nvalues for the mainland Asteraceae. However, this data on many thousands of\nspecies does not exist. Further, island traits in our review are scored at the radiation\nlevel, not individual species.\n● Thank you for the suggestion on improving the figure. We increased the font of the\nkey in panel C.\nMinor comments:\nLine 29: I think Carlquist's Island Biogeography should be cited here, it was incredibly\nimportant work.\n● We agree. Carlquist’s Island Biology (1974) has been cited several times throughout\nthe manuscript but we have now also referenced it here in the introduction as a\nfoundational work on islands.\nLine 56: I would also include cushion forms.\n● Great point and we agree; cushion forms are a fascinating habit (especially of some\niconic island Asteraceae, i.e. Raoulia) and have now been included in the diversity of\ngrowth forms list.\n● The according sentence now reads (lines 49-51): “Members of the family exhibit\ngreat variation in growth habit: from small annual herbs to woody perennial shrubs,\nlianas, and trees; cushion forms and succulents; and even, in rare cases, epiphytic\nand aquatic plants.”\nLine 153: Could you please explain better what the trait \"botanical continent\" means?\n● Yes, we have added a description of the variable to clarify the “botanical continent”\nframework.\n● (Lines 421-423) “We extracted the following variables: latitude and longitude, …\nbotanical continent (level 1, standardized biogeographic scheme for recording plant\ndistributions defined by the Biodiversity Information Standards (TDWG)), and biome\n(Ecoregions) (Dinerstein et al., 2017).”\nLine 249: What was the threshold used in the VIF analysis?\n● Thanks for the comment, we have defined our VIF threshold (<5) in the text.\n● (Lines 520-521) “To validate the fitted models, we checked for collinearity in\npredictors via variance inflation factor (VIF) scores, with a threshold of less than five,\nand checked the residuals with the DHARMA package (Hartig, 2022).”\nLine 527: I think greater care must be taken when comparing Asteraceae to other groups,\nlike birds. There are over twice as many composites as birds and by chance we should\nexpect there to be more cases of island radiations.\n● This is a great point. We have added a sentence to highlight this (lines 346-349):\n“However, some of those groups are much less diverse than Asteraceae (e.g.\napproximately 11,000 bird species compared to the c. 33,000 Asteraceae species),\nso whether the propensity to radiate is also exceptionally higher in Asteraceae\nremains to be investigated.”\nReviewer #2\nThe paper by Roeble et al. looks into the diversity of Asteraceae in islands. I really enjoyed\nreading this manuscript, I think it is very well written and the methods are comprehensive. To\nmy knowledge, this is the first study that looks into the insular diversity of this mega-diverse\nfamily on a global scale. The results show that despite Asteraceae being the most species\nrich family of plants, it is not the most specious on islands. It also shows how species\nrichness increases with area of the island but decreases with isolation, whereas number of\nsingle-island endemics increase with both area and isolation.\n● Thank you for your positive comments and review. We have incorporated all of your\ncomments below, which have helped clarify some of our key points and we have now\nexpanded the discussion on traits in the radiation results.\nI only have a couple of small comments.\nResults and Discussion, line 334. “Asteraceae are also underrepresented on oceanic islands\ngiven their overall diversity”. The meaning of this was not clear to me. Do you mean not well\nsampled, identified, or understudied?\n● We have rephrased this sentence to clarify this point:\n● (Lines 128-131) “On oceanic islands, Asteraceae are the most diverse family for both\nthe number of native and endemic species. Yet, despite high species richness\ncompared to other families, Asteraceae diversity on oceanic islands is lower than\nexpected given their diversity globally (Figure 1B).”\nLine 522. “How the overall number of island radiations within Asteraceae compares to other\nflowering plant families still remains unknown”. I thought that is what you did in this study.\nIsn’t one of the questions of this paper “How does the island diversity of Asteraceae\ncompare with that of other families?”. Please clarify.\n● We compared the diversity (i.e. species richness) of Asteraceae on islands with other\nangiosperm families by compiling global checklists of all families and then comparing\nisland diversity to null expectations. These results answered our first question “(1)\nHow does the island diversity of Asteraceae compare with that of other flowering\nplant families?”. Regarding the radiations specifically, we only reviewed the insular\nradiations (confirmed and putative) for Asteraceae to answer our fourth question “(4)\nHow many island radiations have occurred within Asteraceae and are there\ncommonalities between radiations?”. A review of island radiations for all flowering\nplant families is beyond the scope of this manuscript. While no comparable review\nhas yet been done on other plant families, we contextualize the results to reviews in\nother taxonomic groups (i.e. birds) and reviews limited in scope (i.e. only radiations\non oceanic islands) further down in the discussion.\n● We appreciate you identifying that this text is not clear and now have updated this\nsection to specify a comparable analysis of island radiations in plants has yet to be\ndone.\n● This section (lines 336-339) now reads: “How the overall number of island radiations\nwithin Asteraceae compares to other flowering plant families still remains unknown\nbecause a comparative analysis of all island radiations has not been conducted.\nHowever, recent reviews of radiations with different scopes or on wider taxonomic\ngroups shed light on the magnitude of Asteraceae radiations on islands revealed\nhere.”\nIn the methods, it is mentioned that you looked into “traits often hypothesized to be\nassociated with island radiations (breeding system, dispersal syndrome, ploidy level,\nhybridization)” (lines 303-305). However, in the discussion there is no mention about your\nfindings on ploidy or hybridization patterns. Did you find anything there worth mentioning?\nHybridization is often seen as one of the drivers of genetic diversity in several insular plant\ngroups, so I’m wondering if it could play a role in Asteraceae as well?\n● Thank you for the comment, we have now expanded the discussion on the traits\nassociated with Asteraceae radiations on islands.\n● (Lines 361-364) “Hybridization and polyploidy are thought to be common features of\nadaptive radiations and linked to plant diversification on islands (Marques et al.,\n2019; Gillespie et al., 2020; Meudt et al., 2021; Cerca et al., 2023), and we found\nthese two traits are to some extent associated with island radiations in Asteraceae:\nboth hybridization and polyploidy are documented in 40% of the confirmed\nradiations.”\nReviewer #3\nThis manuscript represents a comprehensive and careful, analytical synthesis of patterns\nand correlates of island diversity and diversification in the most diverse family of flowering\nplants, Asteraceae. The results advance understanding of island biogeography significantly\nby revealing unexpected hotspots of diversity within a global perspective and demonstrating\nthat this family of plants, which is often regarded as exceptional and therefore possibly\nunhelpful for explaining broader-scale biogeographic phenomena, in fact conforms to\nexpected biogeographic rules and is therefore an excellent subject for studying\nbiogeographic phenomena in general (as concluded by the authors). Equally importantly, the\nstudy serves to highlight a large diversity of genera worldwide that are understudied and\nwarrant close attention as putative radiations that may hold important secrets for island\nbiology. Perhaps most of all, this study has generated a significant diversity of resources,\nsuch as global lists and traits of island composites, that will serve researchers going forward\nand will ensure that it is a go-to reference for future investigations, thus magnifying its impact\nand citation. I enthusiastically recommend its publication.\n● Thank you for the very positive evaluation of our manuscript and your valuable\nsuggestions.\nMinor suggestions/corrections:\nLine 43: “biogeographical rates” is perhaps a bit unclear as to what is being included here.\n● Good point; we now give examples of the biogeographic rates to improve clarity.\n● (Lines 38-39) “These studies reveal how links between island features (e.g. area,\nisolation, age, climate), functional traits (e.g. insular woodiness), and biogeographical\nrates (e.g. colonization, speciation, extinction) are important determinants of the\nnumber of native and endemic species of flowering plants on islands….”\nLine 52--53: There are two naturalized species of Asteraceae now known from Antarctica, so\nprobably best to change “occur on” to “are native to” here.\n● We have updated this sentence to be more precise.\n● (Lines 46-49) “Species of this family are native to every continent except Antarctica\nand are found in a wide range of habitats, but are most abundant in dry and semi-arid\nhabitats and in Mediterranean-type ecosystems, deserts, grasslands, and mountains\n(Funk et al., 2009).”\nLine 70: In addition to capacity for selfing, it may be worth noting that self-incompatible\nisland composites (including representatives of some of the more diverse island radiations,\nsuch as taxa of Dendroseris, Scalesia, etc.) have sporophytic SI, where dominance\nrelationships among S-alleles may allow for some degree of selfing and inbreeding more\ngenerally, which may facilitate both establishment after dispersal and retention of genetic\ndiversity under insular conditions, favoring adaptation (Crawford et al. 2009, already in the\nreferences, could be cited for this point, but especially see a just-released review of\nreproductive biology in oceanic-island Asteraceae by Crawford et al. 2024 Bot Rev). The\nauthors note later in the manuscript that data are still sparse on breeding systems across the\nfamily, and that point is very well taken.\n● Thank you for your suggestion and expertise on this topic. We expanded the\nintroduction on factors facilitating Asteraceae success in colonizing and establishing\non islands to also include functionally self-incompatible colonizers and now reference\nthe new review by Crawford.\n● (Lines 60-67) “Their success in dispersal, establishment, and diversification on\nislands has been suggested to result from a combination of intrinsic factors [...], and\nthey are capable of several breeding systems that favor establishment on islands.\nMany island species are self-compatible (Grossenbacher et al., 2017), while species\nin several island lineages are functionally self-incompatible with the capacity to\nself-seed and a genetic system (i.e. sporophytic self-incompatibility) that aids both in\nthe establishment of small populations and the retention of genetic diversity after\narrival (Crawford et al., 2024).”\nLines 325-327: The finding of lower-than-expected species diversity of Asteraceae on\nislands based on overall species diversity in the family was also concluded by a recent\nanalysis of island disharmony (König et al. 2021) that is already in the references and could\nbe cited here.\n● This is a great point that will improve the presentation of our results. We have now\nincluded a small discussion to contextualize our results with the recent study by\nKönig et al., 2021 on island disharmony in plants.\n● This according section (lines 121-124) now reads: “These results align with a recent\nstudy focused on island disharmony in plants (König et al., 2021), which found that\nwhile Asteraceae are generally under-represented on islands given their species\nrichness in mainland source pools, the family is nonetheless pervasive on islands.”\nFig. 3: The position of Abrotanella shown here is accidentally indicated by an arrow and in\nthe caption as belonging to tribe Astereae, rather than to tribe Senecioneae, where all\nevidence places it (and where it is indicated as belonging in the supplementary data).\n● Thank you for picking up on this mistake. We have now corrected Figure 3 and made\nadditional improvements: Abrotanella is now correctly associated with Senecioneae\non the figure and in the legend; and we added an illustration of Commidendrum\nrugosum from Saint Helena to represent Astereae.\nTable S4: The column headings “Subfamily” and “Tribe” are reversed here.\n● The S4 table headings have now been corrected.\nReviewer: Bruce G. Baldwin\nReviewer #4\nThis is an impressive contribution towards the understanding of plant diversity on islands\nand specially of mega diverse Compositae.\nThe text reads very well and the excellent figures complement brilliantly the thorough\ncompilation of information and results presented in the article. This is a contribution worthy of\npublication. My comments are only minor and are detailed as follows.\n● We thank the reviewer for their very positive evaluation and valuable suggestions.\nPage 2, lines 49-50\nWhen providing aka names, Compositae should appear first. Notice that this is a standard\nscientific name, not the common name used on line 50 as “composite”\n● This is a great point. We have updated the syntax of this sentence to highlight\nCompositae as the alternative scientific name.\n● (Lines 44-45) “Asteraceae (Compositae), commonly known as the daisy or sunflower\nfamily, boast the greatest species number of any plant family in the world..”\nPage 3, line 74.\nThe sentence start alluding to two studies, but only one is cited. I understand authors refers\nalso to the one mentioned in line 75… but it is a bit confusing nonetheless.\n● We have restructured the sentence to clarify this:\n● (Lines 71-73) “Two recent studies, one reviewing adaptive radiations across flowering\nplants (Schenk et al., 2021) and another focused on adaptive radiations on oceanic\nislands across all taxonomic groups (Cerca et al., 2023), both found Asteraceae to be\noverrepresented in terms of adaptive radiations compared to other clades.”\nPage 3, line 77\nPerhaps it is an editorial policy behind the lack of authors on scientific names, but these\nnames MUST have authority the first time they appear on text.\n● While we agree that taxonomic authority at the first reference of the name is\nimportant, we are following the journal’s editorial standard of only italicizing species\nnames and not including authority.\nPage 7, line 289\nCheck citation syntax\n● We updated the citation formatting to the numerical style, so each reference is now\nuniquely identified.\nPage 12, Figure 3\nPlant drawing # 3 with some minor re-arrangements of #1 and #2 could be conveniently\nplaced next to the Senecioneae bar\n● Thank you for the suggestion. We attempted to rearrange the illustrations in Figure 3\nto place species adjacent to their respective tribes, but this required longer crossing\narrows. We opted for the simplified layout with the illustration of Senecioneae on the\nbottom referenced by corresponding numbers. We recognize this is not ideal, but\nhope the visualization displays the results/information in a clear (and aesthetic) way.\n● Additionally, we updated Figure 3 to correct a mistake identified by Reviewer 3 and\nwe also added a new illustration of Commidendrum rugosum from Saint Helena to\nrepresent Astereae.\nPage 16, line 512\nReplace “6” with six. Please check throughout text as there are several other instances that\nneed such replacements.\n● We have standardized the text so that all general, whole numbers ten and under are\nspelled out."}, {"round": 2, "reviewer_comments": {"reviewer_1": "This is my second review of the Roeble et al. manuscript \"Asteraceae in Isolation: Diversity and Island Biogeography of the Largest Plant Family.\" In my first review, I brought up several key issues that I asked the authors to address. In reading their comments and the second draft of the manuscript, I feel quite satisfied in the authors' responses to my concerns and I do view this draft of the manuscript as being much stronger. I only have a couple of very minor corrections to bring up and I list them below.\nMinor issues:\nThe semicolons on lines 50 are a bit odd to read and the sentence could be rewritten as a list to avoid them.\nPlease be more consistent in the number of species in Asteraceae. It was reported as 32,000–34,000, then 33,000, then 33,994. I recommend finding a number and sticking with it.\nOn line 184 the term \"apomixis\" is used and then defined. Strictly speaking, their definition is correct, but I recommend applying a better definition so that non-botanists will be able to understand the term. In particular, I would make sure to say that this is the production of seeds without fertilization.", "reviewer_2": "The authors have done a great job addressing all the comments from my initial review and I have no further comments to add. I think this paper is an important contribution to understand diversification patterns in Asteraceae and a significant contribution to the field of insular biogeography in general."}, "author_response": "Response to Reviewers’ Comments\nRevision 2\nReviewer #1\nThis is my second review of the Roeble et al. manuscript \"Asteraceae in Isolation: Diversity\nand Island Biogeography of the Largest Plant Family.\" In my first review, I brought up several\nkey issues that I asked the authors to address. In reading their comments and the second\ndraft of the manuscript, I feel quite satisfied in the authors' responses to my concerns and I\ndo view this draft of the manuscript as being much stronger. I only have a couple of very\nminor corrections to bring up and I list them below.\n● Thank you for reviewing our manuscript. Your comments in both reviews have\nenhanced and strengthened our paper.\nMinor issues:\nThe semicolons on lines 50 are a bit odd to read and the sentence could be rewritten as a\nlist to avoid them.\n● We have restructured this sentence to improve clarity: “Members of the family show\ngreat variation in growth habit and range from small annual herbs to woody perennial\nshrubs, lianas, and trees. Additionally, some species exhibit specialized habits such\nas cushion forms, succulents, and even, in rare cases, are epiphytic and aquatic\nplants.”\nPlease be more consistent in the number of species in Asteraceae. It was reported as\n32,000–34,000, then 33,000, then 33,994. I recommend finding a number and sticking with\nit.\n● We have updated the manuscript throughout for consistency in reporting the overall\ndiversity of Asteraceae.\nOn line 184 the term \"apomixis\" is used and then defined. Strictly speaking, their definition is\ncorrect, but I recommend applying a better definition so that non-botanists will be able to\nunderstand the term. In particular, I would make sure to say that this is the production of\nseeds without fertilization.\n● We appreciate this suggestion and have adjusted the sentence to now read:\n“Apomixis, a mode of asexual reproduction in which seeds are produced without\nfertilization, is a poorly understood trait in Asteraceae (Noyes 2007) and one that\nchallenges taxonomic species concepts and delimitation (Haveman 2013).”\nReviewer #2\nThe authors have done a great job addressing all the comments from my initial review and I\nhave no further comments to add. I think this paper is an important contribution to\nunderstand diversification patterns in Asteraceae and a significant contribution to the field of\ninsular biogeography in general.\n● Thank you for your thorough and positive review of our manuscript. We appreciate\nyour time, expertise, and valuable comments."}]

Decision letter