Andrew B. Leslie

Hemisphere-scale differences in conifer evolutionary dynamics

Fundamental differences in the distribution of oceans and landmasses in the Northern and Southern Hemispheres potentially impact patterns of biological diversity in the two areas. The evolutionary history of conifers provides an opportunity to explore these dynamics, because the majority of extant conifer species belong to lineages that have been broadly confined to the Northern or Southern Hemisphere during the Cenozoic. Incorporating genetic information with a critical review of fossil evidence, we developed an age-calibrated phylogeny sampling ∼80% of living conifer species. Most extant conifer species diverged recently during the Neogene within clades that generally were established during the later Mesozoic, but lineages that diversified mainly in the Southern Hemisphere show a significantly older distribution of divergence ages than their counterparts in the Northern Hemisphere. Our tree topology and divergence times also are best fit by diversification models in which Northern Hemisphere conifer lineages have higher rates of species turnover than Southern Hemisphere lineages. The abundance of recent divergences in northern clades may reflect complex patterns of migration and range shifts during climatic cycles over the later Neogene leading to elevated rates of speciation and extinction, whereas the scattered persistence of mild, wetter habitats in the Southern Hemisphere may have favored the survival of older lineages.

Flotation preferentially selects saccate pollen during conifer pollination

• Among many species of living conifers the presence of pollen with air bladders (saccate pollen) is strongly associated with downward-facing ovules and the production of pollination drops. This combination of features enables saccate pollen grains captured in the pollination drop to float upwards into the ovule. Despite the importance of this mechanism in understanding reproduction in living conifers and in extinct seed plants with similar morphologies, experiments designed to test its effectiveness have yielded equivocal results. • In vitro and in vivo pollination experiments using saccate and nonsaccate pollen were performed using modeled ovules and two Pinus species during their natural pollination period. • Buoyant saccate pollen readily floated through aqueous droplets, separating these grains from nonbuoyant pollen and spores. Ovules that received saccate pollen, nonsaccate pollen or a mixture of both all showed larger amounts and higher proportions of saccate pollen inside ovules after drop secretion. • These results demonstrate that flotation is an effective mechanism of pollen capture and transport in gymnosperms, and suggest that the prevalence of saccate grains and downward-facing ovules in the evolutionary history of seed plants is a result of the widespread use of this mechanism.

Explaining the distribution of breeding and dispersal syndromes in conifers

The evolution of plants exhibiting different sexes, or dioecy, is correlated with a number of ecological and life-history traits such as woody growth form and animal-dispersed seeds, but the underlying causes of these associations are unclear. Previous work in seed plants has suggested that the evolution of fleshy cones or seeds may favour dioecy. In this study, we use a well-sampled molecular phylogeny of conifers to show that although dioecy and fleshiness strongly co-occur at the species level, this relationship has not resulted from numerous separate origins of this trait combination or from differential rates of diversification. Instead, we suggest that two character combinations—the ancestral dry-monoecious condition and the derived fleshy-dioecious condition—have persisted in conifers longer than other combinations over evolutionary time. The persistence of these trait combinations appears to reflect differences in the rate of successful transition into and out of these character states over time, as well as the geographical restriction of species with rare combinations and their consequent vulnerability to extinction. In general, we argue that such persistence explanations should be considered alongside ‘key innovation’ hypotheses in explaining the phylogenetic distribution of traits.

THE PALEONTOLOGICAL CONTEXT OF ANGIOSPERM VEGETATIVE EVOLUTION

Angiosperms represent more than three-quarters of all land plant species despite existing for only a quarter of land plant history, inspiring much interest in understanding what aspects of angiosperm biology may have enabled their unparalleled success. However, comparative study of extant plants cannot fully address the basis of angiosperm dominance because most living nonflowering plants are members of recently radiating lineages as young or younger than the flowering plants and, thus, are a highly biased sampling of the full 400 Myr history of vascular plant diversity. Here, a survey of the fossil record demonstrates that most anatomical traits that are now unique to the angiosperms were more broadly distributed among extinct lineages. However, the growth capacities of angiosperms are likely to have been uniquely high for all of vascular plant history and may have enabled a greater range of architectural possibilities, including the fast-growing annual herbs that represent a large proportion of angiosperm diversity. Many of the gymnosperm lineages lost to extinction during the angiosperm radiation may have been understory and earlier successional plants with advantages relative to conifers for early establishment but without the capacity to match either the high leaf area of mature conifers or the high productivity per unit leaf area of angiosperms. Vascular plants had already occupied all terrestrial climate zones before the angiosperm radiation, but the spread of flowering plants may have substantially changed the vegetation structure of many ecosystems and may have actually changed the temperature and rainfall patterns that determine ecosystem distributions.

Whole-plant reconstruction and phylogenetic relationships of Elatides Zhoui Sp. nov. (Cupressaceae) from the early cretaceous of Mongolia

Premise of research. Exceptionally well-preserved lignified fossils from the Early Cretaceous of Mongolia include abundant conifer leafy shoots with attached pollen cones and seed cones. A whole-plant reconstruction based on these fossils enables a critical evaluation of the relationship of this extinct plant with extant conifers. Methodology. Bulk lignite samples collected from the Tugrug lignite mine were disaggregated in water, cleaned with hydrochloric and hydrofluoric acids, washed, and dried in air. Fossils were then examined using light and scanning electron microscopy. Pivotal results. Elatides zhoui sp. nov. has helically arranged leaves with two narrow lateral stomatal bands, predominantly on the adaxial leaf surface. Pollen cones are usually borne laterally on shoots in tight spirals; each microsporophyll bears three pollen sacs that produce nonsaccate pollen with a small circular aperture. Seed cones have numerous bract-scale complexes, each with a small membranous ovuliferous scale and four to six seeds. Elatides zhoui is the most completely understood of all described Elatides species, and major features of seed cone and pollen cone morphology indicate that it is most closely related to extant Cunninghamia, which today has two species restricted to East Asia. Morphological cladistic analyses using parsimony resolved an expanded Cunninghamioideae clade, which includes extant Cunninghamia, E. zhoui, and other Cunninghamia-like fossils, as the sister group to all other extant Cupressaceae sensu lato. Conclusions. Elatides zhoui provides further evidence for the diversity of Cupressaceae sensu lato during the Cretaceous and supports the hypothesis that cunninghamioid conifers in particular were diverse and widespread during the early evolution of the Cupressaceae.

Shifting functional roles and the evolution of conifer pollen-producing and seed-producing cones

Abstract Exploring patterns in the evolution of seed plant reproductive morphology within a functional context offers a framework in which to identify and evaluate factors that potentially drive reproductive evolution. Conifers are a particularly useful group for studies of this kind because they have a long geologic history and their reproductive organs are borne on separate structures with discrete functions. Multivariate analysis of morphological data collected from pollen-producing and seed-producing cones of Paleozoic, Mesozoic, and extant conifer species shows that seed cones underwent a significant expansion of morphological diversity that began during the Early–Middle Jurassic and has continued into the present day. In contrast, pollen cones show significantly lower levels of morphological diversity and exhibit similar basic morphologies throughout conifer evolutionary history. The increase in seed cone diversity through time is primarily the result of two novel structural and organizational features that evolved independently in different conifer families during the Mesozoic: robust, tightly packed cones in members of Araucariaceae, Cupressaceae sensu lato, and Pinaceae, and highly reduced, fleshy cones or solitary seeds in Podocarpaceae, Taxaceae, and some members of Cupressaceae sensu stricto. In extant conifers, these cone morphologies are associated with species that have strong interactions with vertebrate seed predators, seed dispersers, or a combination of both. This suggests that increases in the strength and complexity of biotic interactions in the Jurassic and Cretaceous were a primary driver of conifer reproductive evolution, and that patterns of character evolution relate to the increasing importance of cone tissue in seed protection and seed dispersal through time.

INTERPRETING THE FUNCTION OF SACCATE POLLEN IN ANCIENT CONIFERS AND OTHER SEED PLANTS

Saccate pollen is present in many ancient seed plants and in two families of extant conifers. In living conifers, saccate pollen occurs in taxa that combine erect ovulate cones at the time of pollination, inverted ovules, and pollination drops. Sacci function primarily to float pollen grains through a liquid pollination drop and concentrate them near the nucellus of the ovule. The morphology and anatomy of sacci are crucial to the proper operation of this pollination mechanism, and similar size proportions in fossil and modern saccate grains suggest that ancient pollen may have functioned in the same way as modern forms. Multivariate analysis of discrete pollen characters performed on data from in situ grains of several groups of fossil seed plants indicates that modern saccus morphology and structure appear as early as the Upper Carboniferous in some nonconiferous seed plants but later in the evolutionary history of the conifer lineage. Combined evidence from pollen morphology suggests that sacci may have functioned in their modern capacity by the Upper Carboniferous in at least some groups of seed plants, which is consistent with the occurrence of potentially inverted ovules in many extinct groups producing saccate pollen. This study also suggests that modern saccus morphology has evolved independently several times over the course of seed plant evolution.

Fossils matter: improved estimates of divergence times in Pinus reveal older diversification

BackgroundThe taxonomy of pines (genus Pinus) is widely accepted and a robust gene tree based on entire plastome sequences exists. However, there is a large discrepancy in estimated divergence times of major pine clades among existing studies, mainly due to differences in fossil placement and dating methods used. We currently lack a dated molecular phylogeny that makes use of the rich pine fossil record, and this study is the first to estimate the divergence dates of pines based on a large number of fossils (21) evenly distributed across all major clades, in combination with applying both node and tip dating methods.ResultsWe present a range of molecular phylogenetic trees of Pinus generated within a Bayesian framework. We find the origin of crown Pinus is likely up to 30 Myr older (Early Cretaceous) than inferred in most previous studies (Late Cretaceous) and propose generally older divergence times for major clades within Pinus than previously thought. Our age estimates vary significantly between the different dating approaches, but the results generally agree on older divergence times. We present a revised list of 21 fossils that are suitable to use in dating or comparative analyses of pines.ConclusionsReliable estimates of divergence times in pines are essential if we are to link diversification processes and functional adaptation of this genus to geological events or to changing climates. In addition to older divergence times in Pinus, our results also indicate that node age estimates in pines depend on dating approaches and the specific fossil sets used, reflecting inherent differences in various dating approaches. The sets of dated phylogenetic trees of pines presented here provide a way to account for uncertainties in age estimations when applying comparative phylogenetic methods.

Predation and protection in the macroevolutionary history of conifer cones

Conifers are an excellent group in which to explore how changing ecological interactions may have influenced the allocation of reproductive tissues in seed plants over long time scales, because of their extensive fossil record and their important role in terrestrial ecosystems since the Palaeozoic. Measurements of individual conifer pollen-producing and seed-producing cones from the Pennsylvanian to the Recent show that the relative amount of tissue invested in pollen cones has remained constant through time, while seed cones show a sharp increase in proportional tissue investment in the Jurassic that has continued to intensify to the present day. Since seed size in conifers has remained similar through time, this increase reflects greater investment in protective cone tissues such as robust, tightly packed scales. This shift in morphology and tissue allocation is broadly concurrent with the appearance of new vertebrate groups capable of browsing in tree canopies, as well as a diversification of insect-feeding strategies, suggesting that an important change in plant–animal interactions occurred over the Mesozoic that favoured an increase in seed cone protective tissues.

Ancient islands acted as refugia and pumps for conifer diversity

Island species are thought to be extinction‐prone because of small population sizes, restricted geographical distribution and limited dispersal ability. However, the topographical and environmental heterogeneity, geographical isolation and stability of islands over long timescales could create refugia for taxa whose source area is threatened by environmental changes. We address this possibility by inferring the evolution of the New Caledonia (NC) and New Zealand (NZ) conifer diversity, which represents over 10% of the worlds diversity for this group. We estimate speciation and extinction rates in relation to the presence/absence on these islands, and dispersal rates between the islands and surrounding areas. We also test the Eocene submersion of NC and the Oligocene drowning of NZ by comparing the fit of biogeographical scenarios using ancestral area estimations. We find that extinction rates were significantly lower for island species, and dispersal “out of islands” was higher. A model including a diversification shift when NC emerged better explains the diversification dynamics. Biogeographical analyses corroborate that conifers experienced high continental extinctions, but survived on islands. NC and NZ have thus contributed to the worlds conifer diversity as “island refugia”, by maintaining early‐diverging lineages from continents during environmental changes on continents. These ancient islands also acted as “species pumps”, providing species into adjacent areas. Our study highlights the important but neglected role of islands in promoting the evolution and conservation of biodiversity.