Recommendation of: The biogeography of evolutionary radiations on oceanic archipelagos. Round#2

Evolutionary radiations on oceanic archipelagos (ROAs) have long served as models for understanding evolutionary and ecological processes underlying species diversification. Yet, diversity patterns emerging from ROAs have received relatively little attention from biogeographers, even though characterizing the effect of key geo-environmental factors on island clade species could be important for unraveling diversification dynamics. In this study, we conducted a comparative analysis using island-specific species richness values for approximately one hundred ROAs across major oceanic archipelagos (mostly Hawaii, Canary Islands, Galápagos and Fiji) and taxa (vascular plants, invertebrates and vertebrates). Our aim was to determine whether (1) ROA species richness patterns scale as a function of key geo-environmental factors including island area, geological age, environmental heterogeneity (elevation and topographic complexity) and inter-island isolation, and (2) whether the magnitude of the effects of these factors varies across archipelagos and taxa. Our results identified elevation as a key driver of ROA species richness patterns on islands, supporting existing theoretical and empirical work that highlighted the central role of environmental heterogeneity in driving diversification on oceanic islands. As importantly, we found that the influence of geo-environmental factors varies across archipelagos and taxa, suggesting that unique archipelagic dynamics and biological traits together shape diversification differently. Our findings emphasize the value of applying biogeographical modeling at the resolution of individual radiations to improve our understanding of evolutionary processes on oceanic archipelagos.

Remote locations, such as oceanic islands, typically harbour relatively few species, some of which go on to generate endemic radiations. Species colonising these locations tend to be a non-random subset from source communities, which is thought to reflect dispersal limitation. However, non-random colonisation could also result from habitat filtering, whereby only a few continental species can become established. We evaluate the imprints of these processes on the Galápagos flora by analysing a comprehensive regional phylogeny for ~39000 species alongside information on dispersal strategies and climatic suitability. We found that habitat filtering was more important than dispersal limitation in determining species composition. This finding may help explain why adaptive radiation is common on oceanic archipelagoes - because colonising species can be relatively poor dispersers with specific niche requirements. We suggest that the standard assumption that plant communities in remote locations are primarily shaped by dispersal limitation deserves reconsideration.

Adaptive radiation is a common evolutionary phenomenon in oceanic islands. From one successful immigrant population, dispersal into different island environments and directional selection can rapidly yield a series of morphologically distinct species, each adapted to its own particular environment. Not all island immigrants, however, follow this evolutionary pathway. Others successfully arrive and establish viable populations, but they remain in the same ecological zone and only slowly diverge over millions of years. This transformational speciation, or anagenesis, is also common in oceanic archipelagos. The critical question is why do some groups radiate adaptively and others not? The Juan Fernández Islands contain 105 endemic taxa of angiosperms, 49% of which have originated by adaptive radiation (cladogenesis) and 51% by anagenesis, hence providing an opportunity to examine characteristics of taxa that have undergone both types of speciation in the same general island environment. Life form, dispersal mode, and total number of species in progenitors (genera) of endemic angiosperms in the archipelago were investigated from literature sources and compared with modes of speciation (cladogenesis vs. anagenesis). It is suggested that immigrants tending to undergo adaptive radiation are herbaceous perennial herbs, with leaky self-incompatible breeding systems, good intra-island dispersal capabilities, and flexible structural and physiological systems. Perhaps more importantly, the progenitors of adaptively radiated groups in islands are those that have already been successful in adaptations to different environments in source areas, and which have also undergone eco-geographic speciation. Evolutionary success via adaptive radiation in oceanic islands, therefore, is less a novel feature of island lineages but rather a continuation of tendency for successful adaptive speciation in lineages of continental source regions.

The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, with ~60 endemic species having originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterised by phenotypic modifications encompassing morphological, metabolic and behavioural changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, D. silvatica, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low coverage-based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high-quality genome, we characterised genome-wide levels of nucleotide polymorphism, divergence and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. We also identified several candidate genomic regions that are potentially under positive selection, highlighting relevant biological processes, such as vision and nitrogen extraction as potential adaptation targets. These processes may ultimately drive species diversification in this genus. This pioneering study of spiders that are endemic to an oceanic archipelago lays the groundwork for broader population genomics analyses aimed at understanding the genetic mechanisms driving adaptive radiation in island ecosystems.

AimAfter colonising isolated islands, many types of plants and animals undergo extreme morphological diversification. In stark contrast, other island taxa change more subtly and converge evolutionarily on intermediate body size (the island rule). This paradox of island evolution has gone undetected for decades, perhaps because each pattern has been investigated separately using different analytical tools. Here, I investigate the paradox of island evolution in the endemic floras of four oceanic archipelagos in the Southwest Pacific.LocationChatham, Kermadec, Lord Howe & Norfolk Islands.TaxonWoody plants.MethodsI test whether the sizes of ‘solitary endemics’ (species that evolved anagenetically in the absence of co‐occurring endemic congeners) are correlated with their closest mainland ancestors. I also test whether island–mainland size relationships in 'solitary endemics' differ from isometry, as predicted by the island rule. Next, I test whether the stature of ‘co‐occurring endemics’ (closely related, often cladogenetic species) exhibits exaggerated differentiation.ResultsThe stature of 'solitary endemics' was correlated with their mainland relatives, and two out of the four archipelagos showed evidence of the island rule. On the other hand, the stature of 'co‐occurring endemics' was unrelated to their closest mainland relatives and often highly differentiated.Main conclusionsOverall results suggest that the island paradox arises from two distinct evolutionary pathways. Solitary endemics evolve more slowly and often converge on intermediate morphology, while co‐occurring endemics evolve more rapidly and often exhibit highly differentiated morphology. Future work aimed at a better understanding of the mechanisms underpinning the island paradox could help to further unite phylogenetic work on adaptive radiations and macroecological tests of the island rule under a single conceptual umbrella.

Fifty-six species of eyeless and reduced-eyed (obligately cryptozoic) macroscopic arthropods are now known from the Galapagos Islands. These occupy cave, ground water, and soil-litter habitats. Sixteen soil-inhabiting species have become established after their probable inadvertent introduction by humans. The number and diversity of the remaining 40 native and endemic species are remarkable because of the geologic youth (about three million years maximum) and oceanic isolation of the islands. Soil habitats contain ten species whose ancestors naturally arrived on the islands in an already eyeless condition, demonstrating that such taxa have greater powers of overwater dispersal than is generally thought. Caves and soils are inhabited by ten eyeless or reduced-eyed species which have related fully-eyed epigean (sister?) species, usually on the same island, indicating relatively recent (possibly parapatric) adaptive radiation into subterranean environments. Another 20 species have no dose Galapagos relatives, and 15 of these are probably relicts of lineages which became extinct in epigean terrestrial habitats, probably because of repeated periods of intense aridity during the Pleistocene. Similar evolutionary patterns exist in the eyeless arthropods of the Hawaiian and Canary archipelagos, indicating that there are common processes in the origins of such eyeless tropical oceanic island faunas.

Evolutionary genomics of oceanic island radiations

Despite numerous, well-documented evolutionary histories of plant groups which underwent rapid radiation in various oceanic archipelagos, very little is known about the genetic basis of species differences and adaptive radiation. This paper represents the first such study in the Macaronesian Islands using non-model endemic plants, the woody Sonchus alliance. Here I inferred the genetic basis of species differences between two Canary Island endemics, the herbaceous perennial, shade tolerant Lactucosonchus webbii and the woody, coastal desert perennial Sonchus radicatus by quantitative trait locus (QTL) mapping using AFLP markers. A total of 23 QTL (7.3-23.8% PVE; phenotypic variance explained) for 11 morphological traits were found, one for flowering time (31% PVE), and five QTL (7-10.7% PVE) for two physiological traits (intrinsic water use efficiency and stomatal conductance). Interpreted cautiously, these results suggest that major morphological and some physiological differences between the two species are controlled by numerous genes with small to moderate effect. This implies that major morphological changes in island plants can be more complex than suggested by other studies, such as in Tetramolopium in the Hawaiian Islands. The genetic basis of arborescence on islands, one of the most spectacular convergent features of plants across different lineages and archipelagos, is also discussed.

The contribution of the Galapagos Islands to increasing our understanding of evolution can hardly be surpassed by any other place of similar size on Earth. Evolutionary biology research on the Galapagos spans studies on the origins of life to molecular phylogeny and evolutionary developmental biology. Most pioneering research conducted on the Galapagos was basic descriptive natural history that focused on the evolutionary ecology of endemic species, with an emphasis on the patterns and mechanisms of adaptation, geographic distribution, and taxonomic affinities, based mostly on appearance and behavior. Modern research, however, such as that conducted by Peter and Rosemary Grant and several other scientists, has made the transition from descriptive patterns to a more quantitative and scientific orientation that features the testing of hypotheses about the evolution and conservation of Galapagos organisms and ecosystems. Now, the study of speciation and adaptive radiation, two common evolutionary processes found on oceanic archipelagos like the Galapagos, can be tracked in time and space, owing to the development of modern molecular genetic techniques and its application to the study of phylogenies (molecular phylogeny) and biography (phylogeography). Island ecosystems and organisms offer a unique opportunity for the study of the fundamental principles of evolution, including natural selection, adaptation, and speciation. Both the Galapagos National Park, as the authority, and scientists deserve much recognition for maintaining the manipulation of organisms and ecosystems at a minimal level to preserve the systems under study. Here, the most relevant subjects on the principles and mechanisms of evolutionary biology are succinctly addressed by research studies conducted in the Galapagos Islands. By no means does the review include all of the fascinating studies that have been conducted since Darwin’s memorable visit to the Galapagos 174 years ago on 16 September 1835.

QuestionsOceanic islands are global hotspots of endemism and evolutionary radiations but many have been severely degraded by human activities and biological invasions. We evaluated the pace and direction of the natural recovery of ecosystems over 77 years across a subtropical oceanic archipelago including islands of various size, elevation, histories of human settlement and deforestation, and invasions by non‐native plants and mammals. This information is essential to guide the ecological restoration of the archipelago.LocationForest vegetation on nine of the Ogasawara Islands in the northwestern Pacific Ocean.MethodsWe first digitized historical vegetation data of the Ogasawara Islands collected during field surveys in 1935. Then, after checking their species compositions, we integrated past and present plant community types. Finally, we identified the landscape‐scale changes in forest vegetation by comparing vegetation maps from 1935, 1979 and 2012.ResultsOver 77 years, the vegetation trajectories of each island varied depending on the introduction of invasive alien species and the remaining proportion of native forest, the latter of which had a strong influence on the recoverability of native forest.ConclusionsOur results highlight the importance of the history of invasive species introductions and the remaining proportion of native forest—both of which reflect the intensity of anthropogenic disturbance—in determining the degree of human intervention needed for restoration on oceanic islands.

Oceanic archipelagos have long been treated as a Petri dish for studies of evolutionary and ecological processes. Like archipelagos, cities exhibit similar patterns and processes, such as the rapid phenotypic divergence of a species between urban and nonurban environments. However, on a local scale, cities can be highly heterogenous, where geographically close populations can experience dramatically different environmental conditions. Nevertheless, we are yet to understand the evolutionary and ecological implications for populations spread across a heterogenous cityscape. To address this, we compared neutral genetic divergence to quantitative trait divergence within three native riparian and four city park populations of an iconic urban adapter, the eastern water dragon. We demonstrated that selection is likely acting to drive divergence of snout‐vent length and jaw width across native riparian populations that are geographically isolated and across city park populations that are geographically close yet isolated by urbanization. City park populations as close as 0.9 km exhibited signs of selection‐driven divergence to the same extent as native riparian populations isolated by up to 114.5 km. These findings suggest that local adaptation may be occurring over exceptionally small geographic and temporal scales within a single metropolis, demonstrating that city parks can act as archipelagos for the study of rapid evolution.

The life and adventures of an eight-legged castaway: Colonization and diversification of Philisca ghost spiders on Robinson Crusoe Island (Araneae, Anyphaenidae)

The adaptive radiation of the Hawaiian honeycreepers is the largest ever recorded for birds on an oceanic archipelago. Despite including >50 species in 21 genera, no hybridizations across honeycreeper species have ever been confirmed. Here, we report genetic and morphological analyses that verify the first hybrid between two Hawaiian honeycreeper species: the 'I'iwi (Vestiaria coccinea) and 'Apapane (Himatione sanguinea). This hybridization is notable given that the parental species diverged ∼1.6 mya and show distinct morphological differences. Further, this discovery is important in light of recent evidence that hybridization plays an important role in speciation and genetic diversity in both plants and animals.

A recommendation of: Baptiste Brée, Thomas J. Matthews, José María Fernandez-Palacios, Christian Paroissin, Kostas A. Triantis, Robert J. Whittaker, François Rigal The biogeography of evolutionary radiations on oceanic archipelagos https://doi.org/10.1101/2024.10.07.616413

A recommendation of: Baptiste Brée, Thomas J. Matthews, José María Fernandez-Palacios, Christian Paroissin, Kostas A. Triantis, Robert J. Whittaker, François Rigal The biogeography of evolutionary radiations on oceanic archipelagos https://doi.org/10.1101/2024.10.07.616413