Peter H. Weston

Phylogenetic biome conservatism on a global scale

How and why organisms are distributed as they are has long intrigued evolutionary biologists. The tendency for species to retain their ancestral ecology has been demonstrated in distributions on local and regional scales, but the extent of ecological conservatism over tens of millions of years and across continents has not been assessed. Here we show that biome stasis at speciation has outweighed biome shifts by a ratio of more than 25:1, by inferring ancestral biomes for an ecologically diverse sample of more than 11,000 plant species from around the Southern Hemisphere. Stasis was also prevalent in transocean colonizations. Availability of a suitable biome could have substantially influenced which lineages establish on more than one landmass, in addition to the influence of the rarity of the dispersal events themselves. Conversely, the taxonomic composition of biomes has probably been strongly influenced by the rarity of species’ transitions between biomes. This study has implications for the future because if clades have inherently limited capacity to shift biomes, then their evolutionary potential could be strongly compromised by biome contraction as climate changes.

Phylogeny of the eudicots : a nearly complete familial analysis based on rbcL gene sequences

A phylogenetic analysis of 589 plastid rbcL gene sequences representing nearly all eudicot families (a total of 308 families; seven photosynthetic and four parasitic families are missing) was performed, and bootstrap re-sampling was used to assess support for clades. Based on these data, the ordinal classification of eudicots is revised following the previous classification of angiosperms by the Angiosperm Phylogeny Group (APG). Putative additional orders are discussed (e.g. Dilleniales, Escalloniales, Vitales), and several additional families are assigned to orders for future updates of the APG classification. The use of rbcL alone in such a large matrix was found to be practical in discovering and providing bootstrap support for most orders. Combination of these data with other matrices for the rest of the angiosperms should provide the framework for a complete phylogeny to be used in macro-evolutionary studies.

Contrasted patterns of hyperdiversification in Mediterranean hotspots.

Dating the Tree of Life has now become central to relating patterns of biodiversity to key processes in Earth history such as plate tectonics and climate change. Regions with a Mediterranean climate have long been noted for their exceptional species richness and high endemism. How and when these biota assembled can only be answered with a good understanding of the sequence of divergence times for each of their components. A critical aspect of dating by using molecular sequence divergence is the incorporation of multiple suitable age constraints. Here, we show that only rigorous phylogenetic analysis of fossil taxa can lead to solid calibration and, in turn, stable age estimates, regardless of which of 3 relaxed clock-dating methods is used. We find that Proteaceae, a model plant group for the Mediterranean hotspots of the Southern Hemisphere with a very rich pollen fossil record, diversified under higher rates in the Cape Floristic Region and Southwest Australia than in any other area of their total distribution. Our results highlight key differences between Mediterranean hotspots and indicate that Southwest Australian biota are the most phylogenetically diverse but include numerous lineages with low diversification rates.

A PHYLOGENETIC STUDY OF POLLINATOR CONSERVATISM AMONG SEXUALLY DECEPTIVE ORCHIDS

Abstract Orchids of the genus Chiloglottis are pollinated through the sexual deception of male wasps mainly from the genus Neozeleboria (Tiphiidae: Thynninae). The orchids mimic both the appearance and sex pheromones of wingless female thynnines but provide no reward to the deceived males. Despite the asymmetry of this interaction, strong pollinator specificity is typical. Such plant‐pollinator interactions would seem to be relatively flexible in the plants adaptive response to variation in the local pollinator resource. However, we present DNA sequence data on both orchids and wasps that demonstrate a pattern of pollinator conservatism operating at a range of taxonomic levels. Sequence data from the wasps indicate 15 of 16 Chiloglottis pollinators are closely related members of one clade of Thynninae. A pattern of congruence between orchid and wasp phylogenies is also demonstrated below the generic level, such that related orchids tend to use related thynnine wasps as specific pollinators. Comparative physiological data on the wasp responses to the floral scents of two Chiloglottis species and one outgroup, Arthrochilus, indicate similar attractive volatile chemicals are used by related orchid taxa. By extension, we infer a similarity of sex pheromone signals among related thynnines. Thus, the conservative pattern of pollinator change in sexually deceptive orchids may reflect phylogenetic patterns in the sex pheromones of their pollinators.

Solar radiation as a factor in the evolution of scleromorphic leaf anatomy in Proteaceae

Species of the major Southern Hemisphere family, Proteaceae, have many scleromorphic anatomical structures in their leaves. Many of these structures (very thick cuticles and five anatomically distinct structures beneath the epidermis) are associated with the leaf surface exposed to direct light. These structures increase the path through which solar radiation must pass before reaching the mesophyll. In this study, such structures are proposed to protect the mesophyll from excess solar radiation, including photosynthetically active, ultraviolet, and possibly infrared radiation. Scleromorphic structures of the upper leaf surface and nonscleromorphic photoprotective structures (dense trichomes and papillae of the upper surface) occur almost exclusively in open vegetation. Open vegetation species of Proteaceae occur in oligotrophic and/or cold and/or dry places, where protection from light in excess of photosynthetic capacity and damage from ultraviolet light should be most important. Data from 123 species and a supertree constructed from available molecular phylogenies are used to show that the proposed photoprotective structures evolved many times within Proteaceae. In tests of correlated evolution, the proposed photoprotective structures are significantly associated with open vegetation, but not with dry habitats.

The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae.

Sunken, covered, and encrypted stomata have been anecdotally linked with dry climates and reduced transpiration and therefore have been used to infer dry palaeoclimates from fossils. This study assesses the evolutionary and ecological associations of such stomatal protection in a model system-the diverse southern hemisphere family Proteaceae. Analyses were based on the morphology of over 1400 Australian, South African, New Caledonian, New Zealand, and South American species, anatomy of over 300 of these species, and bioclimatic data from all 1109 Australian species. Ancestral state reconstruction revealed that five or six evolutionary transitions explain over 98% of the dry climate species in the family, with a few other, minor invasions of dry climates. Deep encryption, i.e., stomata in deep pits, in grooves, enclosed by tightly revolute margins or strongly overarched by cuticle, evolved at least 11 times in very dry environments. Other forms of stomatal protection (sunken but not closely encrypted stomata, papillae, and layers of hairs covering the stomata) also evolved repeatedly, but had no systematic association with dry climates. These data are evidence for a strong distinction in function, with deep encryption being an adaptation to aridity, whereas broad pits and covered stomata have more complex relations to climate.

The Population Structure and Floral Biology of Amborella Trichopoda (Amborellaceae)

The shrubs and small trees of Amborella trichopoda are functionally unisexual and the populations are dioecious, male biased, and occur primarily in clumps. Floral size dimorphism reported for this species was confirmed by differences in floral biomass. At the level of the inflorescence, there were significantly greater numbers of male versus female flowers/inflorescence. No differences were observed between male and female plants in height, stem number, and diameter at the ground level. Male flowers bear 6 to 21 stamens and female flowers 3 to 6 spirally arranged carpels and staminodes that mimic the fertile androecia in male flowers. Flowering within a population was synchronous, and flowers of Amborella trichopoda are both insect- and wind-pollinated. A wide variety of insects ranging in size from ca. 1 mm to 7 cm in length pollinate the flowers, indicating a generalist pollination system. Beetles involved in pollination dwell in the forest litter but also spend hours on the leaves, flowers, and branches feeding on pollen. Pollen is the reward for insects as there is an absence of detectable floral volatiles and nectars, and anthers lack secretions or food bodies. A free-flowing stigma secretion was occasionally present, but it was not consumed by pollinators. Structural studies indicate that the stigma is of the dry-type, and the pollinators probably visit female flowers because of the mimetic role of the staminodes. The combination of wind and insect pollination exhibited in A. trichopoda is rare in basal angiosperms. Gall midges, parasitoid wasps, and thrips utilize floral tissue as a breeding site, impeding reproduction. Two species of gall-inducing midges (Cecidomyiidae) insert egg(s) into the gynoecia of developing flower buds, converting one or more ovaries into galls. Parasitoid wasps (Chalcidae) lay eggs in the galls that develop into larvae that prey upon the midge maggots. The Cecidomyiidae expanded with the angiosperms, but the earliest fossils of gall-inducing gall midges occur in the Miocene. Deceptive mechanisms involving numerous floral traits in small bisexual and unisexual flowers are common in the ANITA group and other basal angiosperms.

Using fossils and molecular data to reveal the origins of the Cape proteas (subfamily Proteoideae).

The angiosperm family Proteaceae is a distinct component of the Cape Floristic Region biodiversity hotspot with 330 endemic species. Phylogenetic analyses of subfamily Proteoideae using sequence data from one nuclear and six plastid loci show that most of this diversity is contained in two distinct Cape floral clades. Molecular dating analyses, using Bayesian and penalized likelihood methods and four phylogenetically supported fossil age constraints, reveal contrasting histories for these two clades. The genus Protea belongs to a lineage that may have been in Africa since the Late Cretaceous but began to diversify in the Cape only 5-18 Myr ago. In contrast, the Leucadendrinae clade presumably arrived in the region no earlier than 46 Myr ago by long-distance dispersal from an Australian ancestor and the extant members of this clade began to diversify in the Cape 22-39 Myr ago. These results join a growing number of case studies that challenge the commonly accepted view that most of the Cape flora radiated synchronously in the Late Miocene and Early Pliocene when a Mediterranean climate settled in the region.

Transmitting tissue architecture in basal-relictual angiosperms: Implications for transmitting tissue origins

Carpel transmitting tissue is a major floral innovation that is essential for angiosperm success. It facilitates the rapid adhesion, hydration, and growth of the male gametophyte to the female gametophyte. As well, it functions as a molecular screen to promote male gametophytic competition and species-specific recognition and compatibility. Here, we characterize the transmitting tissue extracellular matrix (ECM) and pollen tube growth in basal-relictual angiosperms and test the hypothesis that a freely flowing ECM (wet stigma) was ancestral to a cuticle-bound ECM (dry stigma). We demonstrate that the most recent common ancestor of extant angiosperms produced an ECM that was structurally and functionally equivalent to a dry stigma. Dry stigmas are composed of a cuticle and primary wall that contains compounds that facilitate the adhesion and growth of the male gametophyte. These compounds include methyl-esterified homogalacturonans, arabinogalactan-proteins, and lipids. We propose that transmitting tissue evolved in concert with an increase in cuticle permeability that resulted from modifications in the biosynthesis and secretion of fatty acids needed for cuticle construction. Increased cuticle permeability exposed the male gametophyte to pre-existing molecules that enabled rapid male gametophyte adhesion, hydration, and growth as well as species-specific recognition and compatibility.

Paleo-Antarctic rainforest into the modern Old World tropics: The rich past and threatened future of the “southern wet forest survivors”

UNLABELLED • PREMISE OF STUDY Have Gondwanan rainforest floral associations survived? Where do they occur today? Have they survived continuously in particular locations? How significant is their living floristic signal? We revisit these classic questions in light of significant recent increases in relevant paleobotanical data.• METHODS We traced the extinction and persistence of lineages and associations through the past across four now separated regions-Australia, New Zealand, Patagonia, and Antarctica-using fossil occurrence data from 63 well-dated Gondwanan rainforest sites and 396 constituent taxa. Fossil sites were allocated to four age groups: Cretaceous, Paleocene-Eocene, Neogene plus Oligocene, and Pleistocene. We compared the modern and ancient distributions of lineages represented in the fossil record to see if dissimilarity increased with time. We quantified similarity-dissimilarity of composition and taxonomic structure among fossil assemblages, and between fossil and modern assemblages.• KEY RESULTS Strong similarities between ancient Patagonia and Australia confirmed shared Gondwanan rainforest history, but more of the lineages persisted in Australia. Samples of ancient Australia grouped with the extant floras of Australia, New Guinea, New Caledonia, Fiji, and Mt. Kinabalu. Decreasing similarity through time among the regional floras of Antarctica, Patagonia, New Zealand, and southern Australia reflects multiple extinction events.• CONCLUSIONS Gondwanan rainforest lineages contribute significantly to modern rainforest community assembly and often co-occur in widely separated assemblages far from their early fossil records. Understanding how and where lineages from ancient Gondwanan assemblages co-occur today has implications for the conservation of global rainforest vegetation, including in the Old World tropics.