The evolution of apomixis in angiosperms: A reappraisal

Abstract

Apomixis, the asexual reproduction via seed, has long been regarded a blind alley of evolution. This hypothesis was based on the assumption that apomixis is an irreversible, phylogenetically derived trait that would rapidly lead to extinction of the respective lineages. However, recent updates of the taxonomic distribution of apomixis in angiosperms suggest an alternative evolutionary scenario. Apomixis is taxonomically scattered and occurs in both early and late branching lineages, with several reversals from apomixis to obligate sex along phylogeny. Genetic control of apomixis is based on altered expression patterns of the same genes that control sexual development; epigenetic changes following polyploidization and/or hybridization may trigger shifts from sexuality to apomixis. Mendelian inheritance confirms the facultative nature and possible reversibility of apomixis to sexual reproduction. Apomixis, therefore, could represent a transition period in the evolution of polyploid complexes, with polyspory in paleopolyploids being a remnant of lost apomixis. In neopolyploids, apomixis helps to overcome sterility and allows for geographical range expansions of agamic polyploid complexes. The facultative nature of apomixis allows for reversal to sexuality and further speciation of paleopolyploid lineages. Thus, apomixis may facilitate diversification of polyploid complexes and evolution in angiosperms.     

Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance

Aluminum phytotoxicity and genetically based aluminum resistance has been studied intensively during recent decades because aluminum toxicity is often the primary factor limiting crop productivity on acid soils. Plants that grow on soils with high aluminum concentrations employ three basic strategies to deal with aluminum stress. While excluders effectively prevent aluminum from entering their aerial parts over a broad range of aluminum concentration in the soil, hyperaccumulators take up aluminum in their aboveground tissues in quantities above 1000 ppm; that is, far exceeding those present in the soil or in the nonaccumulating species growing nearby. In between these two extremes are indicator species, representing intermediate responses. A list of aluminum hyperaccumulators in angiosperms is compiled on the basis of data in the literature. Aluminum hyperaccumulators include mainly woody, perennial taxa from tropical regions. Recent molecular phylogenies are used to evaluate the systematic and phylogenetic implications of the character. As was hypothesized earlier, our preliminary conclusions support the primitive status of aluminum hyperaccumulation. According to the APG classification system, this phytochemical character is found in approximately 45 families, which belong largely to the eudicots. Aluminum hyperaccumulators are particularly common in basal branches of fairly advanced groups such as rosids (Myrtales, Malpighiales, Oxalidales) and asterids (Cornales, Ericales, Gentianales, Aquifoliales), but the character has probably been lost in the most derived taxa. The feature is suggested to characterize approximately 18 families (e.g., Anisophylleaceae, Cunoniaceae, Diapensiaceae, Memecylaceae, Monimiaceae, Rapateaceae, Siparunaceae, Vochysiaceae, and several monogeneric families). In 27 other families, aluminum hyperaccumulation is restricted to subfamilies, tribes, or genera. Further analyses of a broader range of taxa are needed to examine the origin and taxonomic significance of aluminum hyperaccumulation in several clades. Aluminum hyperaccumulation provides an evolutionary model system for the integration of different biological disciplines, such as systematics, ecology, biogeography, physiology, and biochemistry. Therefore, multidisciplinary approaches are needed to make further progress in understanding the biology of aluminum hyperaccumulators.     

Avian reproduction: role of ecology in the evolution of cooperative breeding

A new comparative analysis of the speciose and socially diverse family of African starlings provides evidence that cooperative breeding has evolved in unpredictable, seasonal environments.     

Gynoecium evolution in angiosperms: Monomery,pseudomonomery, and mixomery

The presence of a gynoecium composed of carpels is a key feature of angiosperms. The carpel is often regarded as a homologue of the gymnosperm megasporophyll (that is, an ovule-bearing leaf), but higher complexity of the morphological nature of carpel cannot be ruled out. Angiosperm carpels can fuse to form a syncarpous gynoecium. A syncarpous gynoecium usually includes a well-developed compitum, an area where the pollen tube transmitting tracts of individual carpels unite to enable the transition of pollen tubes from one carpel to another. This phenomenon is a precondition to the emergence of carpel dimorphism manifested as the absence of a functional stigma or fertile ovules in part of the carpels. Pseudomonomery, which is characterized by the presence of a fertile ovule (or ovules) in one carpel only, is a specific case of carpel dimorphism. A pseudomonomerous gynoecium usually has a single plane of symmetry and is likely to share certain features of the regulation of morphogenesis with the monosymmetric perianth and androecium. A genuine monomerous gynoecium consists of a single carpel. Syncarpous gynoecia can be abruptly transformed into monomerous gynoecia in the course of evolution or undergo sterilization and gradual reduction of some carpels. Partial or nearly complete loss of carpel individuality that precludes the assignment of an ovule (or ovules) to an individual carpel is observed in a specific group of gynoecia. We termed this phenomenon mixomery, since it should be distinguished from pseudomonomery.     

Hydrophilous pollination and breeding system evolution in seagrasses: a phylogenetic approach to the evolutionary ecology of the Cymodoceaceae

COX, P. A. & HUMPHRIES, C. J. 1992. Hydrophilous pollination and breeding system evolution in seagrasses: a phylogenetic approach to the evolutionary ecology of the Cymodoceaceae. A phylogenetic analysis of seagrasses of the Cymodoceaceae shows the Cymodoceaceae to be monophyletic and Posidoniaceae to be their sister group. Information on the pollination ecologies and breeding systems of the various genera of the Cymodoceaceae were plotted onto the consensus tree obtained for the group. From this analysis, it is suggested that the clade composed of the Zosteraceae, Posidoniaceae and Cymodoceaceae evolved from a freshwater hydrophilous ancestor that developed submarine pollination and filiform pollen in association with invasion of the marine environment. Dioecism and surface pollination appear to have evolved in the progenitor of the Cymodoceaceae, and hence the seagrasses of the Cymodoceaceae are dioecious due to common descent rather than to convergent evolutionary processes in extant genera.     

A tale of four stories: soil ecology, theory, evolution and the publication system

Background

Soil ecology has produced a huge corpus of results on relations between soil organisms, ecosystem processes controlled by these organisms and links between belowground and aboveground processes. However, some soil scientists think that soil ecology is short of modelling and evolutionary approaches and has developed too independently from general ecology. We have tested quantitatively these hypotheses through a bibliographic study (about 23000 articles) comparing soil ecology journals, generalist ecology journals, evolutionary ecology journals and theoretical ecology journals.

Findings

We have shown that soil ecology is not well represented in generalist ecology journals and that soil ecologists poorly use modelling and evolutionary approaches. Moreover, the articles published by a typical soil ecology journal (Soil Biology and Biochemistry) are cited by and cite low percentages of articles published in generalist ecology journals, evolutionary ecology journals and theoretical ecology journals.

Conclusion

This confirms our hypotheses and suggests that soil ecology would benefit from an effort towards modelling and evolutionary approaches. This effort should promote the building of a general conceptual framework for soil ecology and bridges between soil ecology and general ecology. We give some historical reasons for the parsimonious use of modelling and evolutionary approaches by soil ecologists. We finally suggest that a publication system that classifies journals according to their Impact Factors and their level of generality is probably inadequate to integrate “particularity” (empirical observations) and “generality” (general theories), which is the goal of all natural sciences. Such a system might also be particularly detrimental to the development of a science such as ecology that is intrinsically multidisciplinary.     

Sexual dimorphism in gender plasticity and its consequences for breeding system evolution

Flowering plants are able to develop gametes throughout their lives. As a consequence, environmental conditions can impact this development and alter a plant's functional gender or the degree to which it achieves fitness through male or female function. Two dimorphic breeding systems are widespread among angiosperm families: gynodioecy (hermaphrodites and females) and dioecy (males and females). Gynodioecy can evolve into dioecy, via loss of female function on the hermaphrodites, or it can remain stable. Here I discuss how developmental plasticity of gender can impact the sex ratio of populations and thereby influence the transition of one breeding system into another. I review studies showing that greater plasticity of fruit production by hermaphrodites as compared with females causes sex ratios among populations to vary in response to environmental conditions, with higher female frequency expected in harsh or low-quality sites. I also review how dioecy may evolve in dry sites to avoid inbreeding and any consequent inbreeding depression. Taken together, these studies show the importance of understanding how ecological development affects functional gender and consequently the evolutionary stability or malleability of dimorphic breeding systems.     

The evolution of floral biology in basal angiosperms

In basal angiosperms (including ANITA grade, magnoliids, Choranthaceae, Ceratophyllaceae) almost all bisexual flowers are dichogamous (with male and female functions more or less separated in time), and nearly 100 per cent of those are protogynous (with female function before male function). Movements of floral parts and differential early abscission of stamens in the male phase are variously associated with protogyny. Evolution of synchronous dichogamy based on the day/night rhythm and anthesis lasting 2 days is common. In a few clades in Magnoliales and Laurales heterodichogamy has also evolved. Beetles, flies and thrips are the major pollinators, with various degrees of specialization up to large beetles and special flies in some large-flowered Nymphaeaceae, Magnoliaceae, Annonaceae and Aristolochiaceae. Unusual structural specializations are involved in floral biological adaptations (calyptras, inner staminodes, synandria and food bodies, and secretory structures on tepals, stamens and staminodes). Numerous specializations that are common in monocots and eudicots are absent in basal angiosperms. Several families are poorly known in their floral biology.     

The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention

Stamens that have lost their primary function of pollen production, or staminodes, occur uncommonly within angiosperms, but frequently fulfill important secondary floral functions. The phylogenetic distribution of staminodes suggests that they typically arise during evolutionary reduction of the androecium. Differences in the genetic control and patterns of stamen loss between actinomorphic and zygomorphic flowers shape staminode development. In clades with actinomorphic flowers, staminodes generally replace an entire stamen whorl and staminode loss seems irreversible. In contrast, in clades with zygomorphic flowers staminodes evolve from a subset of the stamens in a whorl and staminodes can reappear in a lineage after being lost (e.g., Cheloneae, Scrophulariaceae). If staminodes do not adopt new functions during androecium reduction they are lost quickly, so that nonfunctional staminodes appear only in recently derived taxa. Alternatively, when staminodes assume new floral roles, either directly or indirectly after a nonfunctional period, they can become integral floral components which perpetuate within clades (e.g., Orchidaceae). Indirect evolution of staminode function allows greater flexibility of function by allowing staminodes to take over roles not performed by stamens, such as involvement in mechanisms to prevent self-pollination and mechanisms of explosive pollination. Multifunctional staminodes characterize lineages with universal or widespread staminodes.     

Floral phyllotaxis in basal angiosperms: development and evolution

To date, molecular developmental studies have focused on vegetative rather than floral phyllotaxis because vegetative shoot apices are technically more tractable than floral apices in model plants. In contrast to evolutionary changes in the phyllotaxis of vegetative shoots, however, changes in floral phyllotaxis appear to have played a major role in angiosperm evolution. Consolidation of a whorled floral phyllotaxis in derived groups allowed synorganization of floral organs and further adaptive radiations. In basal angiosperms, floral phyllotaxis is more flexible. To study these phenomena, we need clarification of the complex relations of both spiral and whorled phyllotaxis with divergence angles, plastochrons, spiral versus simultaneous initiation of organs, parastichies, orthostichies, organ series, and whorls. Improved resolution of phylogenetic relationships and increased knowledge of the diversity of floral phyllotaxis will allow us to trace evolutionary changes in floral phyllotaxis in ever more detail. Already, such surveys have confirmed that floral phyllotaxis was unusually labile early in angiosperm evolution. Whether the original floral phyllotaxis in angiosperms was spiral or whorled is equivocal, but it appears that spiral floral phyllotaxis in Magnoliales and Laurales is derived rather than primitive.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution

The postgenomics era will bring many changes to ecology and evolution. Information about genomic sequence and function provides a new foundation for organismal biology. The crucifer Arabidopsis thaliana and its wild relatives will play an important role in this synthesis of genomics and ecology. We discuss the need for model systems in ecology, the biology and relationships of crucifers, and the molecular resources available for these experiments. The scientific potential of this model system is illustrated by several recent studies in plant–insect interactions, developmental plasticity, comparative genomics and molecular evolution.     

Stomatal architecture and evolution in basal angiosperms

Stomatal architecture-the number, form, and arrangement of specialized epidermal cells associated with stomatal guard cells-of 46 species of basal angiosperms representing all ANITA grade families and Chloranthaceae was investigated. Leaf clearings and cuticular preparations were examined with light microscopy, and a sample of 100 stomata from each specimen was coded for stomatal type and five other characters contributing to stomatal architecture. New stomatal types were defined, and many species were examined and illustrated for the first time. Character evolution was examined in light of the ANITA hypothesis using MacClade software. Analysis of character evolution, along with other evidence from this study and evidence from the literature on fossil angiosperms and other seed plant lineages, suggests that the ancestral condition of angiosperms can be described as anomo-stephanocytic, a system in which complexes lacking subdidiaries (anomocytic) intergrade with those having weakly differentiated subsidiaries arranged in a rosette (stephanocytic). From this ancestral condition, tangential divisions of contact cells led to the profusion of different types seen in early fossil angiosperms and Amborellaceae, Austrobaileyales, and derived Chloranthaceae, while the state in Nymphaeales is little modified. Formation of new, derived types by tangential division appears to be a recurrent theme in seed plant evolution.