https://orcid.org/0000-0003-0613-7633
Plant reproduction is a critically important research area that has been well represented in Annals of Botany throughout its long history. As a leader in the field once said to the Chief Editor, ‘if you can’t reproduce, you have no business in the next generation’. With the many threats to the Earth’s flora posed by anthropogenic global change, the study of plant reproduction has taken on new urgency (Parmesan and Hanley, 2015). In short, the phases of the lifecycle that are the most vulnerable in a normal setting are becoming particularly vulnerable in a global change setting, with the consequence that the future business of many plant species could be at risk. In recognition of this, Annals of Botany (AoB) has commissioned a special issue on plant reproduction and global change, scheduled for completion in 2024 (see academic.oup.com/aob), and sponsors symposia and plenaries along the same theme, for example at Botany 2023 (https://2023.botanyconference.org/symposia.html). In addition to these special initiatives, AoB regularly publishes important work on the reproductive biology of plants, with most issues having a paper or two on the subject. Occasionally, we receive a cluster of papers which allow us to bundle them into an issue focusing on plant reproduction, which we have done here for Issue #1 of Volume 132. Focus issues better attract attention to the contributed papers, and in the case of the present issue, provides a suitable opportunity to introduce a new cover format for AoB, the first since January of 1997.
In this Focus on Plant Reproduction, we present seven research papers and a commentary, beginning with a Research in Context review by Sasidharan et al. (2023) that addresses responses of florivores and pollinators to floral volatiles (FVOCS). Floral volatiles can either attract or repel animals, and for the plant they can serve as a chemical means of mediating interactions with mutualists and antagonists in their environment. FVOCs can be used to attract preferred mutualists, notably pollinators, while simultaneously deterring florivores who consume floral parts and reduce reproductive success. Sasidharan et al. provide a timely review of the trade-offs between FVOC production and their benefit. In addition, they take advantage of the Research-in-Context format offered by AoB to combine their literature review with results from an original analysis of interactions between insects and higher plant FVOCs. Research-in-Context articles at AoB are a hybrid of review and original results, and thus provide authors an opportunity to better establish the context and significance of their findings. To complement the literature review, Sasidharan et al. conducted meta-analyses of 55 studies presenting electrophysiological or physiological responses of insects to FVOCS. Notably, their analysis showed that florivores can detect a wider range of FVOCS than pollinators. This result, they hypothesize, could reflect different co-evolutionary imperatives facing pollinators versus florivores. In the case of pollinators, long periods of evolutionary specialization may have conferred tolerance of noxious volatiles, leading to loss of sensitivity. For florivores, maintaining high sensitivity to potentially dangerous anti-herbivore compounds can prevent harmful exposure. Sasidharan et al. also explore putative relationships between FVOCs and pollen chemicals. This is a pertinent enterprise, given pollen constitutes a key food source for insects, and pollen contain a wide diversity of nutritious and noxious compounds (Roulston et al., 2000; Hanley et al. 2008). Synthesising data from 49 plant species, they not only report a negative association between FVOCs and pollen chemical richness, suggesting a trade-off, but that more protein-rich pollen may also contain more toxins. Their findings show that understanding chemodiversity as mediator of interactions is essential for understanding the consequences of plant-insect disruptions in future environments. This may be especially important when survival depends upon how replacement pollinators, or florivores, respond to the chemical cues produced by exotic plants migrating into their environment, or alternatively, how exotic insects react to native plants with a different FVOC profile than plants in the insect’s home environment.
The first original research article in the Focus Issue is an examination of sexual reproduction in two moss species by Bisang et al. (2023). Reproduction in mosses and other bryophytes is often overlooked and undervalued, perhaps because the simplicity of their reproductive system seems straightforward compared to the expensive reproductive effort of angiosperms with their showy flowers and engorged fruits. Mosses by contrast, reproduce via spores formed in simple sporophytic capsules, but only so long as free water is available for sperm to swim from male antheridia to female archegonia and effect fertilization. Given sperm are tiny, and sexually compatible mating types may be some distance off, the challenges at this crucial step in the life cycle are immense, setting up the possibilities for evolutionary innovation. In their study, Bisang et al. examined two mosses distributed from northern to southern Scandinavia. The northern populations of each species rely on clonal reproduction to a much greater degree than southern populations where dispersal via spores is common—a pattern that mimics geographic distributions of self-fertilising (Grossenbacher et al., 2015) and asexual plants (Johnson et al., 2010). Their question was whether sex ratios would change with latitude, in part because greater degrees of sexual reproduction should favour less biased sex ratios. Clonal reproduction may be selected for more strongly at high latitude, because it confers reproductive assurance, which is beneficial under the threat of high extinction rate. Surprisingly, in both species, Bisang et al. observed sex ratios are heavily biased towards the female condition regardless of the rate of sexual reproduction. To explain this pattern, they hypothesise the female biased sex ratios result from greater vegetative spread of female clones relative to male clones. In the accompanying Commentary, Dorken (2023) notes that female biased sex ratios may arise in part from females being the more attractive sex to arthropods, who might facilitate sperm transfer in an example of animal-mediated gamete dispersal in a non-seed plant. This adds an interesting level of reproductive complexity in mosses that is not generally considered by botanists. Dorken further notes how Bisang et al. improve our understanding of the causes of female-bias sex ratio in mosses, and how patterns of sexual selection can differ between bryophytes and flowering plants.
One of the world’s leading moss clades is Sphagnum (peat moss), which dominate mires and bogs of the boreal and cool temperate latitudes through their ability to form extensive peat mats throughout northern North America and Eurasia. Peatlands have received much attention in recent years because they store vast amounts of organic carbon, but are nonetheless, vulnerable to climate warming and drainage, which degrade carbon in the bogs, releasing large amounts of methane or CO2. Many aspects of Sphagnum reproductive biology remain unknown, however, including variability in asexual versus sexual reproduction, and sex ratio expression in the haploid phase of the lifecycle. Shaw et al. (2023) examine reproductive patterns in four closely related species of the Sphagnum magellanicum complex from North America, showing three of the species have female dominated sex ratios, whereas the fourth is male dominated. Intriguingly, variability in sex ratio was not associated with the degree of clonal propagation. Asexual reproduction by vegetative spread is common in Sphagnum species, allowing for sustained populations should climate warming disrupt sexual reproduction. However, if heavy reliance on clonal reproduction reduces genetic diversity in Sphagnum populations, it could reduce Sphagnum resilience in a warming climate, such that peatlands might be more prone to collapse. Studies such as Shaw et al. (2023) are providing critical insights on Sphagnum reproduction that help our understanding of potential risks to peatlands in coming decades, and in turn, potential impacts on the global carbon cycle.
Floral morphology and flower colour often form the first imprint people have of specific plant species, and the unique beauty we find in plant reproductive structures become fixtures in our gardens and landscaping, in our household decorations, and even as the patterns on our adornments. Botanical beauty is typically brought into our lives via floral morphology. Through breeding, humans now engage in an artificial selection experiment with our preferred flowering species. Originally, however, floral characteristics are the result of many generations of co-evolutionary interactions between plants and their pollinators, with the structural features of the flower being finely tuned to match specifics of pollinator size, shape, physiology and behaviour, in addition to selection outcomes that deter unwanted visitors and optimise cost-benefit ratios of plant reproduction (van der Kooi et al., 2021). With the power of molecular phylogenetics, we can now address evolutionary hypotheses regarding adaptive evolution of floral traits, and in turn, how the properties and behavior of pollinators have been influenced by flower evolution. Two papers in this issue use the power of molecular phylogenetics to understand morphological adaptation in flowers. Kiel et al. (2023) take advantage of high morphological diversity in flowers of species of species in the Justiciinae (Acanthaceae) to show that differences in anther properties (thecae separation) are correlated with corolla morphology across the phylogeny of Western Hemisphere Justiciinae. In this clade, hummingbird pollination has evolved four times from ancestral bee/fly pollination. In switching to hummingbird pollination, the plant species acquired stamens with parallel thecae, while the ancestral bee or fly pollinated species have divergent thecae in the anthers. Kiel et al. (2023) hypothesise the floral structures are selected as a suite of characters during major evolutionary shifts, such as the switch to hummingbird pollination. In the genus Thalictrum of the Ranunculaceae, there have been multiple independent transitions between insect and wind pollination, which enables comparative studies on the evolution of floral morphologies during the transitions between biotic and abiotic pollination (Timerman and Barrett, 2019; Wang et al., 2019). Martinez-Gómez et al. (2023) suggest there are positive correlations between the type of pollination and the lengths of key reproductive parts, notably the styles, stigmas, filaments and anthers, with the shorter structures present in insect-pollinated flowers and the longer in wind pollinated flowers. This paper adds to recent Thalictrum work, some of which was published in AoB by the same lab (Wang et al., 2019). Martinez-Gómez et al. hypothesise that repeated convergence on similar morphotypes in Thalictrum reflects specialisation from a mixed ancestral mode of pollination, perhaps by different evolutionary paths.
Nectar is critical to our understanding of plant reproduction as it is both the reward for pollinators, but a pot of gold for robbers and thieves. The expense is therefore not simply in making it, but also defending it from unwanted visitors and microbes. Which strategies of nectar production will work best and cost the least?, Maldonado et al. (2023) examined how visitation rates of bumblebees responded to variability in nectar offerings, using artificial floral displays to present the bumblebees with the same overall nectar amount per display, but in contrasting arrangements. One artificial display provided a constant amount of nectar per flower, while others provided variable amounts, with some flowers having more and others less than the mean present in all flowers in the experiment. They observed the bumblebees visited floral displays presenting variable loads of nectar per flower more often than they visited displays where each flower offered the same amount of nectar. They conclude the bees are more attracted to flowers providing the highest nectar loads, even though the overall display contained many low nectar flowers. By varying the nectar content of their flowers, Maldonaldo et al. show that plants use variable nectar loads to manipulate pollinators, and in doing so, achieve greater numbers of visits at lower net cost than if they consistently produced identical loads of nectar per flower. A similar behaviour from human society is exhibited by merchants, who find that offering a few choice deals can bring in the customers, even though the rest of the merchandise is nothing special.
A critical question in global change science is how well species will be able to migrate to higher latitudes and altitudes as climates warm (Parmesan & Hanley 2015). Migration is not simply a matter of a plant extending its range as the fundamental niche expands, but also requires the range expansion of the reproductive potential; pollinators will either move with the host plants, or alternatively, the host plants must attract a novel set of pollinators in their new range. An excellent opportunity to evaluate the dual migration of hosts and pollination services is offered by the northward migration of mangroves along the Florida coast. In recent decades, mangrove species have been rapidly expanding their range northward as lethal winter cold moderates due to anthropogenic climate warming (Osland et al., 2013; Cavanaugh et al., 2014). To evaluate migration of reproductive potential, Nathan and Gruner (2023) examined how well pollination services migrated northward with rapidly expanding populations of the black mangrove (Avicennia germinans) in northern Florida. They observed no apparent decline in pollination success in the mangroves, but this was not because of equivalent migration of the original pollinating species. Instead, new communities of pollinators formed from pre-existing guilds of insects in the expanded range. Nathan and Gruner conclude that understanding migration will require not just the consideration of pollinator and host migrations, but also an appreciation of the ability of pre-existing or novel communities of insects to provide pollinator services as plants such as mangroves enter a new community. The plant’s dependence on and specialization for different types of pollinators is of course a key element for plant success. If pollinators cannot migrate or be recruited from resident populations, selection may begin to favour abiotic means of pollination, such as the wind-pollinated species of Thalictrum studied by Martinez-Gómez et al. (2023).
Finally, this first issue of Volume 132 marks the introduction of a new cover format for Annals of Botany. We retire the prior format after 27 years of continuous service, making it the second longest running AoB cover style in the journal’s history (the longest is the 1910 to 1937 cover, by six months over the 1997 to 2023 cover; Jackson, 2016). Our reasons for the change are two-fold. First, we wish to publish compelling images submitted by our authors in a large-page format. The previous use of an inset to publish author-supplied images restricted the image size which often led to loss of detail. Second, the full-page background used from 1997 to this year, though often stunning, frequently dominated the author’s image in the inset, contrary to our desire to emphasize the contributed images. Thus, we decided a change was in order.
Examples of AoB covers used over the past 86 years are shown in Fig. 1 (see Jackson, 2015 and 2016 for examples of all covers prior to 1991). Pre-1971 covers were business-like in that they simply listed the journal title and editors or table of contents against a uniform background of grey, brown or white. Plant science journals in general used simple single- or dual-toned covers prior to the 1970s, due to the relatively high cost of printing in colour. Cover styles began to change in the 1970s with the introduction of brightly-coloured covers, as shown by the AoB styles used between 1971 and 1991. The improvement in reproduction quality and lowering of relative printing costs enabled publishers to use colour on journal covers, at first in relatively simple single or two-toned formats, but by the mid-to-late 1990s, using photographs and author supplied images as shown by the AoB cover style introduced in 1997. Today, high-definition, full-page coloured images are the norm for journal covers, especially after journals end their print runs and switch to electronic-only publishing formats.
Eighty-six years of Annals of Botany cover formats, from 1937 to 2023. These covers represent the entire run of the New Series of Annals of Botany, which followed the original series begun in 1887. See Jackson (2015) and (2016) for examples of all cover styles from 1887 to 2012. The 1971-1986 cover style was modified to list Short Communications (1975-1984), or the editorial board members (1985-1986). From 1991, a monochrome cover (1991-1996) and then full colour (1997 onward) was used, and the journal size increased from 17x25 cm to a larger 21x28 cm format. From 1991 to 2023, a different inset image drawn from an article in the issue was used, and from 1997, it was superimposed on a yearly changing image with a green background. From mid 2023 (Vol. 132) onward, each issue will have a single large cover image. Scans and cover images were compiled by T Schwarzacher and RF Sage.
With the expanded cover possibilities enabled by the new format, we invite all authors to submit images and artwork to AoB for consideration as the cover image for the issue in which they publish their work. Author-supplied cover images should be submitted to the AoB editorial office when their article is accepted. Cover submissions should be visually compelling, with good composition, focus and clarity. For example, photographs with high depth of field will often provide excellent results. All botanical subjects will be considered, to include images of habitats, vegetative and reproductive organs, anatomical or cellular features, and diagrams of research results. For further information on cover submissions, see the Annals of Botany website. Authors whose submission is accepted as a cover will receive a poster of the cover for their personal use.
FUNDING
CJvdK is funded by the German Humboldt Foundation.
ACKNOWLEDGEMENTS
We thank Dr Trude Schwarzacher for help in preparing Fig. 1, and Dr Mick Hanley for editorial feedback.
