Plants Of Oceanic Islands Research Articles

Collections‐based systematics and biogeography in the 21st century: A tribute to Dr. Vicki Funk

Collections‐based systematics and biogeography in the 21st century: A tribute to Dr. Vicki Funk

The importance of historical ecology for interpreting evolutionary processes in plants of oceanic islands

AbstractOceanic islands and archipelagos are natural laboratories for investigating patterns and processes of evolution. Islands change with the course of time, resulting in a dynamic ontogeny over millions of years. The combined forces of tectonic plate subsidence and erosion from waves, wind, and rainwater bring about substantial geomorphological change over millions of years, until islands eventually disappear under the sea. Added to these long‐term natural changes to the environment of the islands are the changes caused by human activities in recent centuries. After humans reach a previously unpopulated island, they utilize the natural resources for their own survival, cutting forests for making houses, boats, and firewood. The size of the human population and the length of time on the island determine the degree of environmental impact. Evolutionary processes in plants of oceanic islands take place during ontogeny of the islands, resulting in population divergence, speciation, and hybridization. Due to the dramatic alterations suffered by many islands over millions of years, the present patterns of distribution and ecology of species within endemic groups may have little to do with the patterns when the species originated. Understanding these environmental changes is fundamental to infer a founder effect, reasons for levels of genetic variation within and among populations, and modes of speciation. Special caution must be exercised while making comparisons between groups located on islands of different geological ages and that have endured differing environmental modifications from humans. Examples are provided from the Juan Fernández Archipelago and Lord Howe Island.

Non-intrusive systematic study reveals mutualistic interactions between threatened island endemic species and points to more impactful conservation

Oceanic islands harbour a disproportionately large share of extinct and endangered birds worldwide and up to about 6,800 highly threatened plants, stressing the urgency for conservation efforts there. However, effective conservation action can only be as sound as the ecological understanding on which it is based. Knowledge about the ecology of threatened birds and plants can be relatively sketchy even in well-studied oceanic islands and this can potentially misdirect or erode conservation actions’ effectiveness. We used camera traps to document vertebrate flower visitors of a threatened, mono-specific endemic oceanic island plant (Roussea simplex) that produces much nectar and which was abundant until the 1930s before declining severely despite its presence mostly within protected areas. We determined proportions of native and alien flower visitors in four populations and characterised their ecological role (e.g. florivore, nectar robber, pollinator) through observations and exclusion experiments alongside experiments to determine seed sets by agamospermy, autogamy, geitonogamy and xenogamy. Five native and three alien vertebrate species visited flowers (N = 5,085 camera trap-hours), 96.6% of visits being from birds. Among endemics, 74–96% of visits were by the Mauritius Bulbul (Hypsipetes olivaceus), a threatened bird able to effect pollination contrary to the other endemic birds. Roussea simplex is primarily xenogamous, producing 2,657 ± 480 seeds, and seed set dropped markedly when the bird was excluded (861.8 ± 91.0 SE, Kruskal-Wallis χ2 = 14.2, p < 0.001). Natural seed set was very low (410.0 ± 85.3 SE) where the bird was locally extinct or very rare. Invasive alien rats (Rattus rattus) and long-tailed macaques (Macaca fascicularis) were important florivores or nectar robbers. Systematic non-intrusive study using camera traps combined with manipulative experiments revealed a mutualism between two relatively well-studied threatened endemic species as well as new threats from alien vertebrates acting as nectar robbers and florivores. Roussea simplex’s major decline within protected areas and its abundant and year round flowering and nectar production point to a major hitherto unrecorded drop in floral resource previously available to at least five endemic species, and particularly to its commonest flower visitor and principal pollinator, the threatened Mauritius Bulbul. These findings exemplify how systematic non-intrusive study of threatened species may radically change conservation managers’ priorities which in the current case should focus primarily on controlling alien rats and macaques and re-instating or reinforcing Bulbul-Roussea mutualism as each would be more impactful than addressing gecko-Roussea mutualism disruption by alien ants which so far was the only recorded threat thought to drive the rapid decline of Roussea simplex. Our study underscores that current conservation efforts should also pay particular attention to medium to longer-term changes in habitat or community composition which may not be obvious from merely considering extent and composition of current habitats.

Island woodiness underpins accelerated disparification in plant radiations.

Summary The evolution of secondary (insular) woodiness and the rapid disparification of plant growth forms associated with island radiations show intriguing parallels between oceanic islands and tropical alpine sky islands. However, the evolutionary significance of these phenomena remains poorly understood and the focus of debate.We explore the evolutionary dynamics of species diversification and trait disparification across evolutionary radiations in contrasting island systems compared with their nonisland relatives. We estimate rates of species diversification, growth form evolution and phenotypic space saturation for the classical oceanic island plant radiations – the Hawaiian silverswords and Macaronesian Echium – and the well‐studied sky island radiations of Lupinus and Hypericum in the Andes.We show that secondary woodiness is associated with dispersal to islands and with accelerated rates of species diversification, accelerated disparification of plant growth forms and occupancy of greater phenotypic trait space for island clades than their nonisland relatives, on both oceanic and sky islands.We conclude that secondary woodiness is a prerequisite that could act as a key innovation, manifest as the potential to occupy greater trait space, for plant radiations on island systems in general, further emphasizing the importance of combinations of clade‐specific traits and ecological opportunities in driving adaptive radiations.

Factors driving adaptive radiation in plants of oceanic islands: a case study from the Juan Fern\xe1ndez Archipelago

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.

Rapid population decline of an endemic oceanic island plant despite resilience to extensive habitat destruction and occurrence within protected areas

Background: Over 10,000 island endemic angiosperms are highly threatened by extinction. Yet, few of these species have the temporal change in their range documented and quantified, particularly within a potentially informative context of a long period of botanical study.Aim: Here, we used Roussea simplex a mono-specific genus endemic to Mauritius, itself an island with long botanical history and advanced habitat destruction extent, to investigate how the distribution and population of this model oceanic island plant changed through time.Methods: All known localities and population size estimates were compiled from published literature, herbarium specimens, surveys and personal communications to estimate changes in population size, extent of occurrence and area of occupancy and investigate main distribution patterns.Results: Roussea simplex survives in nine high elevation sites. Since the 1930s, its range halved relative to its maximum known distribution and its population size decreased much faster than direct habitat loss would predict. It now qualifies as Endangered according to the IUCN Red List categories.Conclusions: Even in an extremely deforested island, endemic plant population decline may be driven more by diminishing habitat quality than diminishing habitat extent. This renders habitat protection alone insufficient, therefore addressing ecological interactions is vital to stem population decline.

Cover

Front cover: The cover image, by Jairo Patiño et al., is of a dense population of Echium wildpretii on La Palma island (Canary Islands, Spain) which forms part of one of the most spectacular oceanic island plant radiations. It is based on the Special Paper A roadmap for island biology: 50 fundamental questions after 50 years of The Theory of Island Biogeography, DOI: 10.1111/jbi.12986. Photo Credit: Jairo Patiño.

A new framework for investigating biotic homogenization and exploring future trajectories: oceanic island plant and bird assemblages as a case study

Studies of biotic homogenization have focused primarily on characterizing changes that have occurred between some past baseline and the present day. In order to understand how homogenization may change in the future, it is important to contextualize the processes driving these changes. Here, we examine empirical patterns of change in taxonomic similarity among oceanic island plant and bird assemblages. We use these empirical cases to unpack dynamic properties of biotic homogenization, thereby elucidating two important factors that have received little attention: 1) initial similarity and 2) the influence of six classes of introduction and extinction events. We use Jaccard's Index to explore the interplay among these factors in determining the changes in similarity that have occurred between human settlement and the present. Specifically, we develop general formulas for changes in similarity resulting from each of the six types of introductions and extinctions, so that the effect of each event type is formulated in terms of initial similarity and species richness. We then apply these insights to project how similarity levels would change in the future if the present patterns of introductions and extinctions continue. We show that the six event types, along with initial similarity, can show dramatically different behavior in different systems, leading to widely variable influences on similarity. Plant and bird biotas have homogenized only slightly to date, but their trajectories of change are highly divergent. Although existing patterns of colonization and extinction might not continue unchanged, if they were to do so then plant assemblages would show little additional change, whereas bird assemblages would become much more strongly homogenized. Our results suggest that moderate changes in similarity observed to date mask the potential for more dramatic changes in the future, and that the interaction among initial similarity and differential introduction and extinction regimes drives these dynamics.

Genetic consequences of cladogenetic vs. anagenetic speciation in endemic plants of oceanic islands.

Adaptive radiation is a common mode of speciation among plants endemic to oceanic islands. This pattern is one of cladogenesis, or splitting of the founder population, into diverse lineages in divergent habitats. In contrast, endemic species have also evolved primarily by simple transformations from progenitors in source regions. This is anagenesis, whereby the founding population changes genetically and morphologically over time primarily through mutation and recombination. Gene flow among populations is maintained in a homogeneous environment with no splitting events. Genetic consequences of these modes of speciation have been examined in the Juan Fernández Archipelago, which contains two principal islands of differing geological ages. This article summarizes population genetic results (nearly 4000 analyses) from examination of 15 endemic species, involving 1716 and 1870 individuals in 162 and 163 populations (with amplified fragment length polymorphisms and simple sequence repeats, respectively) in the following genera: Drimys (Winteraceae), Myrceugenia (Myrtaceae), Rhaphithamnus (Verbenaceae), Robinsonia (Asteraceae, Senecioneae) and Erigeron (Asteraceae, Astereae). The results indicate that species originating anagenetically show high levels of genetic variation within the island population and no geographic genetic partitioning. This contrasts with cladogenetic species that show less genetic diversity within and among populations. Species that have been derived anagenetically on the younger island (1-2 Ma) contain less genetic variation than those that have anagenetically speciated on the older island (4 Ma). Genetic distinctness among cladogenetically derived species on the older island is greater than among similarly derived species on the younger island. An important point is that the total genetic variation within each genus analysed is comparable, regardless of whether adaptive divergence occurs.

Δ 6-Desaturase sequence evidence for explosive Pliocene radiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)

The oceanic islands of Macaronesia provide an ideal temporal and spatial context to test hypotheses of plant evolution using a novel set of phylogenetic markers, Δ 6-desaturase sequences. In contrast to the limited resolution of standard molecular markers (nrDNA and plastid sequences), the Δ 6-desaturase sequence phylogeny of Echium unequivocally reconstructs its active colonization across islands and archipelagos (Madeira, the Canary Islands, and Cape Verde), as well as its subsequent geographical and ecological speciation. Molecular-clock estimates using penalized likelihood and Bayesian inference reveal two radiation processes coincident with two dramatic climatic changes recorded in the region: the advent of the cold Canarian sea current (ca. 4 Ma) and the establishment of a strong seasonality in the Pleistocene (1.8 Ma). Though Echium had available all the diversity of present-day Macaronesian environments (xeric and mesic scrub, laurisilva, pine forest, and subalpine habitats) in the Miocene, evolutionary divergence appears to have been triggered by an extension of fluctuating xeric and mesic habitats with the advent of Pliocene conditions. These Echium radiations not only fulfill traditional predictions of adaptive radiation (i.e., common ancestry, rapid speciation, and phenotype–environment correlation), but also, uniquely among Macaronesian species, trait utility of woodiness. A Pliocene transition from annuality to a bush or tree-like condition occurred in early Echium lineages. Maintenance of woodiness in major lineages, and reversal to an herbaceous condition by three independent events, is reported for the first time in plants of oceanic islands.

Mapping Unexplored Genomes: A Genetic Linkage Map of the Woody Sonchus Alliance (Asteraceae: Sonchinae) in the Macaronesian Islands

As an initial step to mapping quantitative trait loci for species differences and adaptive radiation of insular endemics in Macaronesia, a genetic linkage map was constructed from an intergeneric backcross between Lactucosonchus webbii and Sonchus radicatus, core members of the tree lettuces in the Macaronesian Islands. A total of 152 amplified fragment length polymorphism markers were mapped into 10 major and 3 minor linkage groups for a total map length of 644 cM with an average distance of 4.53 cM for the 10 major groups. The genetic linkage map length is considerably less than the estimated, and this may reflect incomplete genomic coverage in the current study or reduced recombination, which is a common feature of maps for hybrids of divergent taxa. Segregation distortion occurred in 34% of the mapped markers, and they were located primarily in 4 linkage groups. Segregation distortion in the current BC(1) intergeneric population is slightly lower than average (40%) for BC(1) interspecific populations. This level of segregation distortion implies that unlike what we normally assume no to few reproductive barriers, oceanic island plant taxa do exhibit some degree of postmating reproductive isolation.

The utility of automated analysis of inter‐simple sequence repeat (ISSR) loci for resolving relationships in the Canary Island species of Tolpis (Asteraceae)

Plants of oceanic islands, often remarkably divergent morphologically from continental relatives, are useful models for studying evolution and speciation because evolution is telescoped in time and space. Prior studies revealed little DNA sequence variation within the clade of ca. 10 Canary Island species of Tolpis, which precluded resolving species relationships. The present study assessed the utility of automated analysis of inter-simple sequence repeat (ISSR) loci for resolving relationships within the clade using 264 individuals from 36 populations of all recognized species and three undescribed morphological variants. Similarity (Dice coefficient) and Fitch parsimony were used to generate neighbor-joining (NJ) and strict consensus trees (MP), respectively. All individuals of the morphologically distinct endemic species formed clusters in both trees. There is also support for clusters of two undescribed variants in the NJ tree. Individuals from a morphologically variable complex consisting primarily of two species are not well resolved at population or species levels. The NJ and MP trees are not congruent at deeper levels, including relationships among species. Results are interpreted in terms of the biology of the species, and the utility of automated analysis of ISSR markers for interpreting patterns of evolution of Tolpis in the Canary Islands is discussed.

Loss of extrafloral nectary on an oceanic island plant and its consequences for herbivory

Two Hibiscus (Malvaceae) species coexist on the oceanic Bonin (Ogasawara) Islands: Hibiscus glaber (an endemic species) and H. tiliaceus (the ancestral non-endemic species). Hibiscus tiliaceus produces extrafloral nectar from the sepals, while H. glaber does not. To clarify the effects of extrafloral nectar loss on Hibiscus-insect relationships, we examined herbivory and insect communities on flower buds of H. glaber and H. tiliaceus. Larvae of the endemic moth Rehimena variegata (Lepidoptera: Pyralidae) attacked 20% of the flower buds on H. glaber, while less than 0.2% of buds on H. tiliaceus were attacked. Introduced species of ants frequently visited the flower buds of H. tiliaceus to collect extrafloral nectar from the sepal, while they rarely visited those of H. glaber. Therefore, extrafloral nectar on H. tiliaceus sepals may function as a facultative defense against flower bud herbivory. The loss of extrafloral nectaries of H. glaber sepals may be related to the original paucity of native herbivores and ants on the Bonin Islands.

Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process.

By their very nature oceanic island ecosystems offer great opportunities for the study of evolution and have for a long time been recognized as natural laboratories for studying evolution owing to their discrete geographical nature and diversity of species and habitats. The development of molecular genetic methods for phylogenetic reconstruction has been a significant advance for evolutionary biologists, providing a tool for answering questions about the diversity among the flora and fauna on such islands. These questions relate to both the origin and causes of species diversity both within an archipelago and on individual islands. Within a phylogenetic framework one can answer fundamental questions such as whether ecologically and/or morphologically similar species on different islands are the result of island colonization or convergent evolution. Testing hypotheses about ages of the individual species groups or entire community assemblages is also possible within a phylogenetic framework. Evolutionary biologists and ecologists are increasingly turning to molecular phylogenetics for studying oceanic island plant and animal communities and it is important to review what has been attempted and achieved so far, with some cautionary notes about interpreting phylogeographical pattern on oceanic islands.