The ontogeny of disparity in Cupressaceae seed cones.

Ontogenetic shape change has long been recognized to be important in generating patterns of morphological diversity and may be especially important in plant reproductive structures. We explore how seed cone disparity in Cupressaceae changes over ontogeny by comparing pollination-stage and mature cones. We sampled cones at pollen and seed release and measured cone scales using basic morphometric shape variables. We used multivariate statistical methods, particularly hypervolume overlap calculations, to measure morphospace occupation and disparity. Cone scales at both pollination and maturity exhibit substantial variability, although the disparity is greater at maturity. Mature cone scales are also more clustered in trait space, showing less overlap with other taxa than at pollination. These patterns reflect two growth strategies that generate closed cones over maturation, either through thin laminar scales or relatively thick, peltate scales, resulting in two distinct regions of morphospace occupation. Disparity patterns in Cupressaceae seed cones change over ontogeny, reflecting shifting functional demands that require specific patterns of cone scale growth. The evolution of Cupressaceae reproductive disparity therefore represents selection for trajectories of ontogenetic shape change, a phenomenon that should be widespread across seed plants.

Quantifying the complexity of plant reproductive structures reveals a history of morphological and functional integration.

Vascular plant reproductive structures have undoubtedly become more complex through time, evolving highly differentiated parts that interact in specialized ways. But quantifying these patterns at broad scales is challenging because lineages produce disparate reproductive structures that are often difficult to compare and homologize. We develop a novel approach for analysing interactions within reproductive structures using networks, treating component parts as nodes and a suite of physical and functional interactions among parts as edges. We apply this approach to the plant fossil record, showing that interactions have generally increased through time and that the concentration of these interactions has shifted towards differentiated surrounding organs, resulting in more compact, functionally integrated structures. These processes are widespread across plant lineages, but their extent and timing vary with reproductive biology; in particular, seed-producing structures show them more strongly than spore or pollen-producing structures. Our results demonstrate that major reproductive innovations like the origin of seeds and angiospermy were associated with increased integration through greater interactions among parts. But they also reveal that for certain groups, particularly Mesozoic gymnosperms, millions of years elapsed between the origin of reproductive innovations and increased interactions among parts within their reproductive structures.

Reproductive innovations and pulsed rise in plant complexity.

Morphological complexity is a notable feature of multicellular life, although whether it evolves gradually or in early bursts is unclear. Vascular plant reproductive structures, such as flowers, are familiar examples of complex morphology. In this study, we use a simple approach based on the number of part types to analyze changes in complexity over time. We find that reproductive complexity increased in two pulses separated by ~250 million years of stasis, including an initial rise in the Devonian with the radiation of vascular plants and a pronounced increase in the Late Cretaceous that reflects flowering plant diversification. These pulses are associated with innovations that increased functional diversity, suggesting that shifts in complexity are linked to changes in function regardless of whether they occur early or late in the history of vascular plants.

Early Cretaceous abietoid Pinaceae from Mongolia and the history of seed scale shedding.

PREMISE: Seed cones of extant Pinaceae exhibit two mechanisms of seed release. In "flexers" the cone scales remain attached to the central axis, while flexing and separating from each other to release the seeds. In "shedders" scales are shed from the axis, with the seeds either remaining attached to the scale or becoming detached. The early fossil history of Pinaceae from the Jurassic to Early Cretaceous is dominated by flexing seed cones, while the systematic information provided by shedding fossil cones has been overlooked and rarely integrated with data based on compression and permineralized specimens. We describe the earliest and best-documented evidence of a "shedder" seed cone from the Aptian-Albian of Mongolia. METHODS: Lignite samples from Tevshiin Govi locality were disaggregated in water, washed, and dried in air. Fossils were compared to material of extant Pinaceae using LM and CT scans. RESULTS: Lepidocasus mellonae gen. et sp. nov. is characterized by a seed cone that disarticulated at maturity and shed obovate bract-scale complexes that have a distinctive ribbed surface and an abaxial surface covered with abundant trichomes. The ovuliferous scale has ca. 30-40 resin canals, but only scarce xylem near the attachment to the cone axis. Resin vesicles are present in the seed integument. Phylogenetic analysis places Lepidocasus as sister to extant Cedrus within the abietoid grade. CONCLUSIONS: The exquisite preservation of the trichomes in L. mellonae raises questions about their potential ecological function in the cones of fossil and living Pinaceae. Lepidocasus mellonae also shows that a shedding dispersal syndrome, a feature that has often been overlooked, evolved early in the history of Pinaceae during the Early Cretaceous.

A novel reproductive strategy in an Early Devonian plant.

Bonacorsi et al. describe a new fossil from the Early Devonian that provides the earliest clear evidence for more advanced reproductive biology in land plants. The plant produced multiple spore size classes, which is an essential innovation necessary for all advanced plant reproductive strategies, including seeds and flowers.

Accumulation over evolutionary time as a major cause of biodiversity hotspots in conifers.

Biodiversity hotspots are important for understanding how areas of high species richness form, but disentangling the processes that produce them is difficult. We combine geographical ranges, phylogenetic relationships and trait data for 606 conifer species in order to explore the mechanisms underlying richness hotspot formation. We identify eight richness hotspots that overlap known centres of plant endemism and diversity, and find that conifer richness hotspots occur in mountainous areas within broader regions of long-term climate stability. Conifer hotspots are not unique in their species composition, traits or phylogenetic structure; however, a large percentage of their species are not restricted to hotspots and they rarely show either a preponderance of new radiating lineages or old relictual lineages. We suggest that conifer hotspots have primarily formed as a result of lineages accumulating over evolutionary time scales in stable mountainous areas rather than through high origination, preferential retention of relictual lineages or radiation of species with unique traits, although such processes may contribute to nuanced differences among hotspots. Conifers suggest that a simple accumulation of regional diversity can generate high species richness without additional processes and that geography rather than biology may play a primary role in hotspot formation.

Not all 'pine cones' flex: functional trade-offs and the evolution of seed release mechanisms.

Seed dispersal is critical for plants, but the evolution of mechanisms that actually release seeds from their parents is not well understood. We use the reproductive cones of conifers, specifically the Pinaceae clade, to explore the factors driving the evolution of different release mechanisms in plants. We combine comparative anatomical and phylogenetic analyses to test whether fundamental trade-offs in the mechanical and hydraulic properties of vasculature underlie the evolution of two seed release mechanisms: cone scale flexion and cone scale shedding. We then test whether these mechanisms are linked with differences in seed size, dispersal syndrome and reproductive allocation. Cone scale xylem in flexing species is tough, but poorly conductive. Xylem in shedding species is less extensive, fragile and highly conductive; its thin-walled tracheids allow scales to easily fracture at maturity. Shedding is also consistently associated with large, densely packed seeds. Pinaceae cones exploit a well-known trade-off in xylem mechanical strength vs hydraulic efficiency to generate release mechanisms that allow seeds of various sizes to leave the protecting cone. The linkage among release mechanisms, vascular anatomy and seed traits illustrates how a wide variety of selective pressures may influence the function and physiology of reproductive structures.

Functional diversity and convergence in the evolution of plant reproductive structures.

Background and Aims: Structures that simultaneously perform many functional roles are likely to show a variety of morphological solutions to these demands, and thus probably exhibit high morphological disparity. In contrast, specialization for a few simple functions should result in a more limited suite of morphologies. We explore this idea using lycopsid reproductive structures, which, throughout their history, have performed a limited set of functional roles compared with the reproductive structures of other plant groups such as seed plants. Methods: We scored living and fossil lycopsid taxa for 18 discrete character measurements and several continuous traits, including sporangium size, supporting axis diameter, and strobilus length and width. We used the discrete characters to construct a multivariate morphospace for lycopsid reproductive morphology through time, and the continuous characters to test whether fossil and extant lycopsids show similar patterns of tissue allocation within reproductive structures. Results: Lycopsids occupy similar areas of reproductive morphospace and show similar patterns of tissue allocation over most of their history, alternating between diffuse fertile zones with leaf-like sporophylls and compact strobili with specialized sporophylls that allow sporangia to be closely packed while also protected during their development. Growth habit also plays an important role in lycopsid reproductive evolution, broadly influencing the size and shape of reproductive structures. Conclusions: Lycopsid reproductive structures are primarily specialized for densely packaging sporangia, and are consistent with the idea that performing limited functional roles is associated with reduced morphological disparity. Morphologies similar to lycopsid strobili are also found in other groups with simple, wind-dispersed propagules, suggesting that the same processes occur across plant lineages.

An overview of extant conifer evolution from the perspective of the fossil record.

PREMISE OF THE STUDY: Conifers are an important living seed plant lineage with an extensive fossil record spanning more than 300 million years. The group therefore provides an excellent opportunity to explore congruence and conflict between dated molecular phylogenies and the fossil record. METHODS: We surveyed the current state of knowledge in conifer phylogenetics to present a new time-calibrated molecular tree that samples ~90% of extant species diversity. We compared phylogenetic relationships and estimated divergence ages in this new phylogeny with the paleobotanical record, focusing on clades that are species-rich and well known from fossils. KEY RESULTS: Molecular topologies and estimated divergence ages largely agree with the fossil record in Cupressaceae, conflict with it in Araucariaceae, and are ambiguous in Pinaceae and Podocarpaceae. Molecular phylogenies provide insights into some fundamental questions in conifer evolution, such as the origin of their seed cones, but using them to reconstruct the evolutionary history of specific traits can be challenging. CONCLUSIONS: Molecular phylogenies are useful for answering deep questions in conifer evolution if they depend on understanding relationships among extant lineages. Because of extinction, however, molecular datasets poorly sample diversity from periods much earlier than the Late Cretaceous. This fundamentally limits their utility for understanding deep patterns of character evolution and resolving the overall pattern of conifer phylogeny.

Why are the seed cones of conifers so diverse at pollination?

Background and Aims: Form and function relationships in plant reproductive structures have long fascinated biologists. Although the intricate associations between specific pollinators and reproductive morphology have been widely explored among animal-pollinated plants, the evolutionary processes underlying the diverse morphologies of wind-pollinated plants remain less well understood. Here we study how this diversity may have arisen by focusing on two conifer species in the pine family that have divergent reproductive cone morphologies at pollination. Methods: Standard histology methods, artificial wind pollination assays and phylogenetic analyses were used in this study. Key Results: A detailed study of cone ontogeny in these species reveals that variation in the rate at which their cone scales mature means that pollination occurs at different stages in their development, and thus in association with different specific morphologies. Pollination experiments nevertheless indicate that both species effectively capture pollen. Conclusions: In wind-pollinated plants, morphological diversity may result from simple variation in development among lineages rather than selective pressures for any major differences in function or performance. This work also illustrates the broader importance of developmental context in understanding plant form and function relationships; because plant reproductive structures perform many different functions over their lifetime, subtle differences in development may dramatically alter the specific morphologies that they use to meet these demands.

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

BACKGROUND: The 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. RESULTS: We 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. CONCLUSIONS: Reliable 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.

Variation in seed size is structured by dispersal syndrome and cone morphology in conifers and other nonflowering seed plants.

Seed size varies tremendously in plants and its evolution is influenced by multiple ecological and biological factors that are difficult to disentangle. In this study, we focus on understanding the role of seed dispersal by animals in the evolution of seed size in conifers, the most diverse extant nonflowering seed plant group. Relationships among seed size, dispersal syndrome, climate and cone morphology were analyzed across conifers using quantitative models of character evolution and phylogenetic regression techniques. Dispersal syndrome is a more consistent predictor of seed size within major extant conifer clades than climate. Seeds are generally larger in animal-dispersed than wind-dispersed species, and particular cone morphologies are consistently associated with specific ranges in seed size. Seed size and cone morphology evolve in a correlated manner in many animal-dispersed conifers, following a trade-off that minimizes the total size of the dispersal unit. These relationships are also present in other nonflowering seed plant groups, and have been important in the evolution of seeds and cones at least over the Cenozoic and perhaps over much of the later Mesozoic.

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 world's 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 world's 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.

Early Cretaceous Umkomasia from Mongolia: implications for homology of corystosperm cupules.

Corystosperms, a key extinct group of Late Permian to Early Cretaceous plants, are important for understanding seed plant phylogeny, including the evolution of the angiosperm carpel and anatropous bitegmic ovule. Here, we describe a new species of corystosperm seed-bearing organ, Umkomasia mongolica sp. nov., based on hundreds of three-dimensionally preserved mesofossils from the Early Cretaceous of Mongolia. Individual seed-bearing units of U. mongolica consist of a bract subtending an axis that bifurcates, with each fork (cupule stalk) bearing a cupule near the tip. Each cupule is formed by the strongly reflexed cupule stalk and two lateral flaps that partially enclose an erect seed. The seed is borne at, or close to, the tip of the reflexed cupule stalk, with the micropyle oriented towards the stalk base. The corystosperm cupule is generally interpreted as a modified leaf that bears a seed on its abaxial surface. However, U. mongolica suggests that an earlier interpretation, in which the seed is borne directly on an axis (shoot), is equally likely. The 'axial' interpretation suggests a possible relationship of corystosperms to Ginkgo. It also suggests that the cupules of corystosperms may be less distinct from those of Caytonia than has previously been supposed.

Integration and macroevolutionary patterns in the pollination biology of conifers.

Integration influences patterns of trait evolution, but the relationship between these patterns and the degree of trait integration is not well understood. To explore this further, we study a specialized pollination mechanism in conifers whose traits are linked through function but not development. This mechanism depends on interactions among three characters: pollen that is buoyant, ovules that face downward at pollination, and the production of a liquid droplet that buoyant grains float through to enter the ovule. We use a well-sampled phylogeny of conifers to test correlated evolution among these characters and specific sequences of character change. Using likelihood models of character evolution, we find that pollen morphology and ovule characters evolve in a concerted manner, where the flotation mechanism breaks down irreversibly following changes in orientation or drop production. The breakdown of this functional constraint, which may be facilitated by the lack of developmental integration among the constituent traits, is associated with increased trait variation and more diverse pollination strategies. Although this functional "release" increases diversity in some ways, the irreversible way in which the flotation mechanism is lost may eventually result in its complete disappearance from seed plant reproductive biology.

Cone size is related to branching architecture in conifers.

The relationship between branch diameter and leaf size has been widely used to understand how vegetative resources are allocated in plants. Branching architecture influences reproductive allocation as well, but fewer studies have explored this relationship at broad phylogenetic or ecological scales. In this study, we tested whether pollen-producing and seed-producing cone size scales with branch diameter in conifers, a diverse and globally distributed lineage of nonflowering seed plants. Branch diameter and cone size were analyzed using multiple regression models and evolutionary models of trait evolution for a data set of 293 extant conifer species within an explicit phylogenetic framework. Branch diameter is a strong predictor of cone size across conifer species, particularly for pollen cones and dry seed cones. However, these relationships are complex in detail because leaf morphology and seed dispersal biology influence the specific ways in which they are expressed. The ubiquity and strength of these scaling relationships across conifers suggest that reproductive and vegetative morphologies are coupled in the group, and it is therefore difficult to disentangle the evolution of cone size from the evolution of branching architecture.

Pinaceae-like reproductive morphology in Schizolepidopsis canicularis sp. nov. from the Early Cretaceous (Aptian-Albian) of Mongolia.

PREMISE OF THE STUDY: Seed cone scales assigned to the genus Schizolepidopsis are widespread in Late Triassic to Cretaceous Eurasian deposits. They have been linked to the conifer family Pinaceae based on associated vegetative remains, but their exact affinities are uncertain. Recently discovered material from the Early Cretaceous of Mongolia reveals important new information concerning Schizolepidopsis cone scales and seeds, and provides support for a relationship between the genus and extant Pinaceae. METHODS: Specimens were collected from Early Cretaceous (probable Aptian-Albian) lignite deposits in central Mongolia. Lignite samples were disaggregated, cleaned in hydrofluoric acid, and washed in water. Specimens were selected for further study using light and electron microscopy. KEY RESULTS: Schizolepidopsis canicularis seed cones consist of loosely arranged, bilobed ovulate scales subtended by a small bract. A single inverted seed with an elongate micropyle is borne on each lobe of the ovulate scale. Each seed has a wing formed by the separation of the adaxial surface of the ovulate scale. CONCLUSIONS: Schizolepidopsis canicularis produced winged seeds that formed in a manner that is unique to Pinaceae among extant conifers. We do not definitively place this species in Pinaceae pending more complete information concerning its pollen cones and vegetative remains. Nevertheless, this material suggests that Schizolepidopsis may be important for understanding the early evolution of Pinaceae, and may potentially help reconcile the appearance of the family in the fossil record with results based on phylogenetic analyses of molecular data.

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.

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.