Insular Woodiness Research Articles

‘Paedomorphosis’ and ‘juvenility’ in secondary xylem: (not such) useful constructs?

Summary In 1962 Carlquist published “A Theory of Paedomorphosis in Dicotyledonous Woods” based on his observations that some species of non-tree growth forms such as stem succulents, lianas, woody herbs, and tree rosettes exhibit, in their secondary xylem, cellular characteristics more commonly associated with primary xylem. He considered the appearance of these characters an expression of protracted juvenility, and that they reflected paedomorphosis. Since then, many others have observed similar suites of traits across multiple plant lineages, as these traits also characterize secondary and insular woodiness, and have used ‘paedomorphic’ and ‘juvenile’ to describe these traits. In this essay, it is argued that the use of the term paedomorphosis should be restricted to cases where ancestor/descendant relationships are known or used in a comparative sense among closely related taxa, to retain its significance as a descriptor of an evolutionary pattern. Second, it is argued that primary growth, and therefore primary xylem, should not be considered ‘juvenile’ because it is not characteristic only of the young, pre-reproductive phases of plant growth but instead persists for the life of the plant. Because both the concepts of juvenility and paedomorphosis possess more or less well-accepted modern meanings that differ in important ways from Carlquist’s use of the terms, a different approach is suggested that focuses on the functional significance of this suit of traits, in addition to their cellular characteristics.

The evolution of insular woodiness

Insular woodiness (IW)-the evolutionary transition from herbaceousness toward woodiness on islands-is one of the most iconic features of island floras. Since pioneering work by Darwin and Wallace, a number of drivers of IW have been proposed, such as 1) competition for sunlight requiring plants with taller and stronger woody stems and 2) drought favoring woodiness to safeguard root-to-shoot water transport. Alternatively, IW may be the indirect result of increased lifespan related to 3) a favorable aseasonal climate and/or 4) a lack of large native herbivores. However, information on the occurrence of IW is fragmented, hampering tests of these potential drivers. Here, we identify 1,097 insular woody species on 375 islands and infer at least 175 evolutionary transitions on 31 archipelagos, concentrated in six angiosperm families. Structural equation models reveal that the insular woody species richness on oceanic islands correlates with a favorable aseasonal climate, followed by increased drought and island isolation (approximating competition). When continental islands are also included, reduced herbivory pressure by large native mammals, increased drought, and island isolation are most relevant. Our results illustrate different trajectories leading to rampant convergent evolution toward IW and further emphasize archipelagos as natural laboratories of evolution, where similar abiotic or biotic conditions replicated evolution of similar traits.

Data and scripts for 'The evolution of insular woodiness'

Data and scripts for 'The evolution of insular woodiness'

Scientists' warning - The outstanding biodiversity of islands is in peril.

Despite islands contributing only 6.7% of land surface area, they harbor ~20% of the Earth’s biodiversity, but unfortunately also ~50% of the threatened species and 75% of the known extinctions since the European expansion around the globe. Due to their geological and geographic history and characteristics, islands act simultaneously as cradles of evolutionary diversity and museums of formerly widespread lineages—elements that permit islands to achieve an outstanding endemicity. Nevertheless, the majority of these endemic species are inherently vulnerable due to genetic and demographic factors linked with the way islands are colonized. Here, we stress the great variation of islands in their physical geography (area, isolation, altitude, latitude) and history (age, human colonization, human density). We provide examples of some of the most species rich and iconic insular radiations. Next, we analyze the natural vulnerability of the insular biota, linked to genetic and demographic factors as a result of founder events as well as the typically small population sizes of many island species. We note that, whereas evolution toward island syndromes (including size shifts, derived insular woodiness, altered dispersal ability, loss of defense traits, reduction in clutch size) might have improved the ability of species to thrive under natural conditions on islands, it has simultaneously made island biota disproportionately vulnerable to anthropogenic pressures such as habitat loss, overexploitation, invasive species, and climate change. This has led to the documented extinction of at least 800 insular species in the past 500 years, in addition to the many that had already gone extinct following the arrival of first human colonists on islands in prehistoric times. Finally, we summarize current scientific knowledge on the ongoing biodiversity loss on islands worldwide and express our serious concern that the current trajectory will continue to decimate the unique and irreplaceable natural heritage of the world’s islands. We conclude that drastic actions are urgently needed to bend the curve of the alarming rates of island biodiversity loss.

Temporal and palaeoclimatic context of the evolution of insular woodiness in the Canary Islands.

Insular woodiness (IW), referring to the evolutionary transition from herbaceousness toward woodiness on islands, has arisen more than 30 times on the Canary Islands (Atlantic Ocean). One of the IW hypotheses suggests that drought has been a major driver of wood formation, but we do not know in which palaeoclimatic conditions the insular woody lineages originated. Therefore, we provided an updated review on the presence of IW on the Canaries, reviewed the palaeoclimate, and estimated the timing of origin of woodiness of 24 insular woody lineages that represent a large majority of the insular woody species diversity on the Canaries. Our single, broad‐scale dating analysis shows that woodiness in 60%–65% of the insular woody lineages studied originated within the last 3.2 Myr, during which Mediterranean seasonality (yearly summer droughts) became established on the Canaries. Consequently, our results are consistent with palaeoclimatic aridification as a potential driver of woodiness in a considerable proportion of the insular woody Canary Island lineages. However, the observed pattern between insular woodiness and palaeodrought during the last couple of million years could potentially have emerged as a result of the typically young age of the native insular flora, characterized by a high turnover.

Parallel evolution of arborescent carrots (Daucus) in Macaronesia.

PremiseDespite intensive research, the pathways and driving forces behind the evolution of derived woodiness on oceanic islands remain obscure. The genus Daucus comprises mostly herbs (therophytes, hemicryptophytes) with few rosette treelets (chamaephytes) endemic to various Macaronesian archipelagos, suggesting their independent evolution. To elucidate the evolutionary pathways to derived woodiness, we examined phylogenetic relationships and the habit and secondary xylem evolution in Daucus and related taxa.MethodsSixty taxa were surveyed for molecular markers, life history, and habit traits. Twenty‐one species were considered for wood anatomical characters. A dated phylogeny was estimated using Bayesian methods. The evolution of selected traits was reconstructed using parsimony and maximum likelihood.Results Daucus dispersed independently to the Canary Islands (and subsequently to Madeira), Cape Verde, and the Azores in the late Miocene and Pleistocene. Life span, reproductive strategy, and life form were highly homoplastic; the ancestor of Daucus was probably a monocarpic, biennial hemicryptophyte. Rosette treelets evolved independently in the Canarian‐Madeiran lineage and in Cape Verde, the latter within the last 0.13 Myr. Treelets and hemicryptophytes did not differ in wood anatomy. Pervasive axial parenchyma in wood occurred more often in polycarpic rather than monocarpic species.ConclusionsLife span and life form in Daucus are evolutionarily labile and may change independently of wood anatomy, which is related to plant reproductive strategy rather than to life form. Insular woodiness may evolve rapidly (as demonstrated in D. bischoffii), and in Daucus, it does not seem to be an adaptation to lower the risk of xylem embolism.

Tracing insular woodiness in giant Daucus (s.l.) fruit fossils from the Early Pleistocene of Madeira Island (Portugal)

AbstractPlants on oceanic islands can evolve insular syndromes such as secondary woodiness, a generalized trend found in island floras worldwide. This phenomenon occurs through evolution in situ. It is triggered by ecological and physiological stimuli that transform herbaceous annuals into woody perennials. However, well‐dated and informative fossils that could help track and frame the evolution of this syndrome are lacking. Remarkably, in Madeira Island (Portugal), there are good examples of Apiaceae that evolved secondary woodiness, like the giant neoendemic Melanoselinum (≡ Daucus). Apiaceae has a very scarce fossil record, despite being a cosmopolitan family and an economically important crop. Here we describe the oldest Daucus s.l. fossil known to date and the first fossil evidence of a plant with insular woodiness. The fossils are preserved as mummified/compressed mericarps within 1.3‐million‐year‐old fluvio‐lacustrine sediments of the Funchal unit, Upper Volcanic complex, near Porto da Cruz. We assign them to the extant neoendemic species Melanoselinum (≡ Daucus) decipiens. The mericarp morphology shows remarkable stasis since the Calabrian stage of the Early Pleistocene. Our results demonstrate that in the Madeiran Daucinae clade, insular woodiness developed at least 1.3 million years ago, indicating a coeval or earlier immigration to Madeira Island of a Daucus sp. Our results reinforce the role of palaeobotanical research in oceanic islands, supported by stratigraphy and geochronology studies, as a key element for the understanding of plant palaeobiogeography, ecology and evolution worldwide. We expect this contribution to shed light on the evolutionary origins of carrots, and related plant groups, an important element of human food, and to better comprehend the evolution of plant insular woodiness.

Island biogeography of the Macaronesian Gesnouinia and Mediterranean Soleirolia (Parietarieae, Urticaceae) with implications for the evolution of insular woodiness

Urticaceae tribe Parietarieae serves as an excellent example to study hypotheses on Macaronesian‐​Mediterranean island biogeography. Parietarieae is distributed in both of these floristically closely related regions and contains two island endemic genera. Gesnouinia is endemic to Macaronesia and was considered a Tertiary relict from a European paleotropical vegetation. This, however, may contradict the general idea of insular woodiness also proposed for this genus. For the origin of the western Mediterranean island endemic Soleirolia, a vicariance scenario, i.e., the split of the Hercynian massif in southern Europe has been suggested. To evaluate these hypotheses and to provide a time frame for island and inter‐island colonization, we applied molecular phylogenetics and dating based on two plastid and one nuclear DNA marker. Additionally, we performed ancestral area reconstruction, analyzed the anatomy of the stem and reconstructed the ancestral character states of woodiness. Our results indicate that Gesnouinia colonized Macaronesia during the Miocene via long‐distance dispersal and may, therefore, be a Tertiary laurel forest relict. Diversification between the laurel forest species Gesnouinia arborea and the rupicolous and more xeric G. filamentosa occurred within Macaronesia during the Pleistocene, possibly due to climate fluctuations. Therefore, G. arborea is not a relict from the Tertiary. Stem anatomy suggests that although woodiness in Gesnouinia likely is derived, it may have evolved prior to island colonization. Soleirolia originated in the Mediterranean during the Miocene. This rules out vicariance from the split of the Hercynian massif in southern Europe during the Oligocene. The divergence of Soleirolia from Majorca, Corsica, Sardinia and the Italian mainland dates to the Pleistocene. This indicates long‐distance dispersal as predominant colonization mode, not ruling out that migration between these areas was possibly facilitated by land bridges during the Pleistocene glaciation cycles.

Evolutionary Comparison of the Chloroplast Genome in the Woody Sonchus Alliance (Asteraceae) on the Canary Islands.

The woody Sonchus alliance consists primarily of woody species of the genus Sonchus (subgenus Dendrosonchus; family Asteraceae). Most members of the alliance are endemic to the oceanic archipelagos in the phytogeographic region of Macaronesia. They display extensive morphological, ecological, and anatomical diversity, likely caused by the diverse habitats on islands and rapid adaptive radiation. As a premier example of adaptive radiation and insular woodiness of species endemic to oceanic islands, the alliance has been the subject of intensive evolutionary studies. While phylogenetic studies suggested that it is monophyletic and its major lineages radiated rapidly early in the evolutionary history of this group, genetic mechanisms of speciation and genomic evolution within the alliance remain to be investigated. We first attempted to address chloroplast (cp) genome evolution by conducting comparative genomic analysis of three representative endemic species (Sonchus acaulis, Sonchus canariensis, and Sonchus webbii) from the Canary Islands. Despite extensive morphological, anatomical, and ecological differences among them, their cp genomes were highly conserved in gene order and content, ranging from 152,071 to 152,194 bp in total length. The number of repeat variations and six highly variable regions were identified as valuable molecular markers. Phylogenetic analysis of 32 species in the family Asteraceae revealed the phylogenetic position of the woody Sonchus alliance within the tribe Cichorieae and the sister relationship between the weedy Sonchus oleraceus and the alliance.

Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought‐induced hydraulic failure than their herbaceous relatives

Abstract Insular woodiness refers to the evolutionary transition from herbaceousness towards derived woodiness on (sub)tropical islands and leads to island floras that have a higher proportion of woody species compared to floras of nearby continents. Several hypotheses have tried to explain insular woodiness since Darwin's original observations, but experimental evidence why plants became woody on islands is scarce at best. Here, we combine experimental measurements of hydraulic failure in stems (as a proxy for drought stress resistance) with stem anatomical observations in the daisy lineage (Asteraceae), including insular woody Argyranthemum species from the Canary Islands and their herbaceous continental relatives. Our results show that stems of insular woody daisies are more resistant to drought‐induced hydraulic failure than the stems of their herbaceous counterparts. The anatomical character that best predicts variation in embolism resistance is intervessel pit membrane thickness (TPM), which can be functionally linked with air bubble dynamics throughout the 3D vessel network. There is also a strong link between TPM vs. degree of woodiness and thickness of the xylem fibre wall vs. embolism resistance, resulting in an indirect link between lignification and resistance to embolism formation. Thicker intervessel pit membranes in Argyranthemum functionally explain why this insular woody genus is more embolism resistant to drought‐induced failure compared to the herbaceous relatives from which it has evolved, but additional data are needed to confirm that palaeoclimatic drought conditions have triggered wood formation in this daisy lineage. A plain language summary is available for this article.

Insular Woodiness on the Canary Islands: A Remarkable Case of Convergent Evolution

Premise of research. One of the most conspicuous aspects of island floras is the relatively high proportion of woody species. Often, but not always, these woody species have developed wood on the islands and have evolved from herbaceous continental ancestors, a phenomenon known as insular woodiness. Shifts from herbaceousness toward increased woodiness also occur on continents (the broader term “secondary woodiness” is more appropriate here and includes insular woodiness), but comprehensive worldwide knowledge about secondary woodiness within angiosperms remains lacking. We update hypotheses regarding the herbaceous ancestry of woody Canarian lineages in a molecular phylogenetic context and investigate the possible link of secondary woodiness and paedomorphic wood features in the Carlquistian sense.Methodology. We have assembled available literature data from molecular phylogenetic studies, wood anatomical descriptions, floras, and taxonomic revisions to identify the native secondarily woody taxa.Pivotal results. In total, at least 220 native Canary Island species of flowering plants, from 34 genera representing 15 families, are truly insular woody. This represents a significant portion of the native nonmonocot angiosperm species on the Canaries, and all of the insular woody species have paedomorphic wood features in the Carlquistian sense, although this wood anatomical syndrome might be more related to particular life forms. The majority of these insular woody groups typically grow in the markedly dry lowland regions, suggesting a possible link between secondary woodiness and increased drought resistance.Conclusions. The Canary Island flora is characterized by at least 38 independent shifts toward insular woodiness, representing an important portion of the endemic angiosperms on the archipelago. These convergent evolutionary events emphasize the remarkable lability in growth forms between herbaceous and woody lineages, but it remains puzzling which environmental variables trigger these shifts and how these independent shifts are regulated genetically.

Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness

See also the Commentary by Rowe and Paul‐Victor

On the origin of the woody buckwheat Fagopyrum tibeticum (= Parapteropyrum tibeticum) in the Qinghai–Tibetan Plateau

Here we tested whether ‘insular woodiness’, a striking evolutionary pattern that commonly occurs on islands, has also appeared in QTP continental endemics. Parapteropyrum, a monotypic shrubby genus occurring in the central QTP, has been previously placed in the tribe Atraphaxideae of the family Polygonaceae, while all the other woody species of this tribe mainly occur in western and central Asia. We studied sequence variations of nuclear ITS (internal transcribed spacer) and cp (chloroplast) DNA ( rbcL and accD) of this genus and the other ten genera. The constructed phylogenies based on ITS, cpDNA or a combination of both datasets, suggest that the woody Parapteropyrum is nested within and most likely evolved from the herbaceous Fagopyrum. We propose that the large-scale uplift of the QTP not only promoted continental species radiation, but also the secondary feature of woodiness in a few herbaceous lineages in response to strong selection pressures, similar to those acting on island flora. In addition, the confirmation of Parapteropyrum within Fagopyrum highlights its potential use as a new, perennial source of buckwheat.

Phylogenetic relationships and evolution of morphological characters in Ononis L. (Fabaceae)

AbstractOnonis L. (Fabaceae, Papilionoideae) is a common genus in the circum‐Mediterranean region. To infer phylogenetic relationships, 69 Ononis species were analyzed using plastid trnL‐F and nuclear ITS DNA sequences. Trees resulting from maximum parsimony analysis and Bayesian inference provide evidence that Ononis is monophyletic but contradict the traditional subgeneric division in O. sects. Ononis and Natrix. However, many of the 22 subsections of the genus are well supported by the molecular data. Phylogenetic reconstructions indicate five major lineages within the genus, which are morphologically supported by peduncle length and flower color, characters which also confirm the polyphyly suggested for O. subsect. Reclinatae. Ononis subsects. Antiquae and Rhodanthae form a basally branching monophylum, confirming the findings of previous studies. An examination of the life strategies dominant in different clades and the climatic conditions in the habitats of the species in the light of the molecular data suggests that O. subsects. Ononis, Mauritanicae and Canariensis are secondarily perennial, with the latter two serving as examples of high altitude woodiness and insular woodiness.

Paedomorphosis, Secondary Woodiness, and Insular Woodiness in Plants

The related concepts of paedomorphosis in the secondary xylem, insular woodiness, and secondary woodiness are reviewed and evaluated in order to clearly distinguish the phenomenon involved, and provide a firm foundation for future research in this area. The theory of paedomorphosis refers to the occurrence of certain juvenile xylem characteristics, such as scalariform perforation plates and lateral wall pitting, in the secondary xylem of shrubby, suffrutescent, pachycaulous, and lianoid growth forms. Paedomorphic characteristics are often found in insular woody species, a fact that has caused paedomorphosis to be associated with secondary woodiness. The anatomy of the secondary xylem in Xanthorhiza simplicissima (Ranunculaceae), Coreopsis gigantea (Asteraceae), and Mahonia bealei (Berberidaceae) is described in order to provide specific data for discussion. These species serve as test cases for the presence of paedomorphosis, and the evolution of secondary woodiness. The secondary xylem of all three species was found to have a degree of paedomorphosis, with Coreopsis having the greatest number of paedomorphic characteristics, Xanthorhiza having an intermediate number, and Mahonia possessing only a single characteristic. Plotting the occurrence of the character states woody and nonwoody on phylogenetic trees containing these taxa shows that Coreopsis is secondarily woody, while the ancestry of the other two species cannot be unambiguously established. These results must, however, be considered preliminary as the occurrence of secondary growth in many “herbaceous” plants often goes unreported. Although paedomorphosis is often associated with secondary woodiness, there are examples of paedomorphic wood in primitively woody taxa. One conclusion is that the degree of paedomorphosis may be a better indicator of the mechanical requirements of the shoot then of its evolutionary history.

Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana

Plants have evolved annual and perennial life forms as alternative strategies to adapt reproduction and survival to environmental constraints. In isolated situations, such as islands, woody perennials have evolved repeatedly from annual ancestors. Although the molecular basis of the rapid evolution of insular woodiness is unknown, the molecular difference between perennials and annuals might be rather small, and a change between these life strategies might not require major genetic innovations. Developmental regulators can strongly affect evolutionary variation and genes involved in meristem transitions are good candidates for a switch in growth habit. We found that the MADS box proteins SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FRUITFULL (FUL) not only control flowering time, but also affect determinacy of all meristems. In addition, downregulation of both proteins established phenotypes common to the lifestyle of perennial plants, suggesting their involvement in the prevention of secondary growth and longevity in annual life forms.

Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae).

Numerous island-inhabiting species of predominantly herbaceous angiosperm genera are woody shrubs or trees. Such "insular woodiness" is strongly manifested in the genus Echium, in which the continental species of circummediterranean distribution are herbaceous, whereas endemic species of islands along the Atlantic coast of north Africa are woody perennial shrubs. The history of 37 Echium species was traced with 70 kb of noncoding DNA determined from both chloroplast and nuclear genomes. In all, 239 polymorphic positions with 137 informative sites, in addition to 27 informative indels, were found. Island-dwelling Echium species are shown to descend from herbaceous continental ancestors via a single island colonization event that occurred < 20 million years ago. Founding colonization appears to have taken place on the Canary Islands, from which the Madeira and Cape Verde archipelagos were invaded. Colonization of island habitats correlates with a recent origin of perennial woodiness from herbaceous habit and was furthermore accompanied by intense speciation, which brought forth remarkable diversity of forms among contemporary island endemics. We argue that the origin of insular woodiness involved response to counter-selection of inbreeding depression in founding island colonies.

Wood Anatomy of Goodeniaceae and the Problem of Insular Woodiness

Wood Anatomy of Goodeniaceae and the Problem of Insular Woodiness