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The Evolutionary Fates of the Four Insect Pollinator Cohorts and Insect Families Hosting Major Vascular-Plant Hosts during the Mid-Cretaceous Angiosperm Radiation
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During the mid-Cretaceous, angiosperms diversified from several nondiverse lineages to their current global domination [1], replacing earlier gymnosperm lineages [2].Several hypotheses explain this extensive radiation [3], one of which involves proliferation of insect pollinator associations in the transition from gymnosperm to angiosperm dominance...
Citations
... This would imply that gymnosperm pollinators were available to angiosperms as they evolved, prior to the first flowering plants. Thus, the co-diversification between insects and angiosperms that we have shown here appears to include, in a wide sense, a pollinator transition of generalist pollen-feeding insects from gymnosperms to angiosperms 32 , as already described in different beetle lineages 35,36 . The marginally non-significant negative correlation with extinction rates in Coleoptera with the rise of angiosperms during the ATR seems to support this idea. ...
Interactions with angiosperms have been hypothesised to play a crucial role in driving diversification among insects, with a particular emphasis on pollinator insects. However, support for coevolutionary diversification in insect–plant interactions is weak. Macroevolutionary studies of insect and plant diversities support the hypothesis that angiosperms diversified after a peak in insect diversity in the Early Cretaceous. Here, we used the family-level fossil record of insects as a whole, and insect pollinator families in particular, to estimate diversification rates and the role of angiosperms on insect macroevolutionary history using a Bayesian process-based approach. We found that angiosperms played a dual role that changed through time, mitigating insect extinction in the Cretaceous and promoting insect origination in the Cenozoic, which is also recovered for insect pollinator families only. Although insects pollinated gymnosperms before the angiosperm radiation, a radiation of new pollinator lineages began as angiosperm lineages increased, particularly significant after 50 Ma. We also found that global temperature, increases in insect diversity, and spore plants were strongly correlated with origination and extinction rates, suggesting that multiple drivers influenced insect diversification and arguing for the investigation of different explanatory variables in further studies.
... Screening rhizosphere soil samples and identifying competent microbial strains is very interesting and applicable [6]. Such strains have been isolated from various environments, including the rhizosphere, saline soil, and limestone mining regions [7][8][9][10]. This diversity of habitats suggests that biofertilizers can adapt to different conditions and be explored for various purposes. ...
As eco-friendly alternative to chemical fertilizers, biofertilizers have gained significance in the quest for sustainable farming. While challenges exist, such as regulatory hurdles and technical complexities, the opportunities in this field are substantial. Understanding rhizosphere engineering can enhance biofertilizers' efficiency, ensuring they provide maximum crop benefits. Genetic engineering of bioinoculants offers a pathway to tailor biofertilizers to specific crop needs, potentially increasing their effectiveness. Multi-trait, multi-strain, and multi-nutrient microbial formulations have the potential to revolutionize the biofertilizer market, allowing for customized solutions that address a range of agricultural needs. These innovations are complemented by market dynamics and the integration of nanotechnology, which can further enhance biofertilizer performance and reach. Such opportunities indicate a bright future for biofertilizer commercialization, where sustainable agriculture can benefit from advanced formulations with an improved understanding of soil-plant interactions. Biofertilizers' prospects are promising, offering a more sustainable and environmentally friendly approach to nourishing the world's growing population.
... [33,34,56]) but little fundamental change in structural complexity. Specialized animal pollination syndromes are also thought to have been common over the Mesozoic [76][77][78] and are associated with high reproductive part type numbers generally [3]. Insect pollination was probably important in the evolution of the most complex gymnosperm reproductive structures; the high part type counts in the bisexual flowers of some extinct bennettitaleans and the staminate strobili of some extant Gnetales (figure 4; electronic supplementary material, figure S3) reflect the presence of both pollen and seed organs as well as enveloping perianth elements. ...
... Pollinators such as moths and bees, which often interact with highly specialized perianth parts and intricate flower geometries, are thought to have diversified with derived angiosperm clades [78] (although see [81]). By contrast, early-diverging angiosperm lineages generally produce less complex flowers and are primarily visited by ovipositing flies and beetles [82], more akin to proposed Mesozoic pollinators [76,77]. These pollination syndromes are thought to rely less on specialized floral geometries and more on cues like odour or food rewards [83]. ...
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.
... There is more direct evidence that a number of insect groups were gymnosperm pollinators in the mid-Mesozoic, indicated by the occasional co-preservation in amber of plausible insect pollinators associated with pollen grains; these finds illustrate the different pathways involving insects in the mid-Cretaceous transition from gymnosperm to angiosperm pollination. Examples from Spanish amber discussed by Peris et al. (2017) include a long-proboscid zhangsolvid fly (specialist dipteran gymnosperm pollinators that were destined to become extinct), thrips (Thysanoptera; gymnosperm pollinators that have maintained this role to the present day) and false blister beetles (Oedemeridaeconsidered 'primitive' gymnosperm pollinators that transferred to angiosperms). Peris et al. (2020b) also report kateridid Coleoptera (short-winged flower beetles) closely associated with pollen from both gymnosperms and a basal angiosperm (water lily) in Myanmar amber, perhaps capturing the early stages of the transition to angiosperm pollination. ...
Amber first became relatively abundant and widespread in the geological record during the Cretaceous period. It originated often as copious resin production by a variety of incompletely understood coniferous trees, generally under humid climates, but not excluding seasonal aridity. Study of insect and other organic inclusions only commenced in the twentieth century, but has expanded considerably since then, with several thousand taxa now described. Cretaceous amber insects can be exquisitely preserved in three dimensions, although tend to be biased towards smaller individuals that lived in the local forest environment. They are therefore complemented by the Cretaceous rock record, which sampled larger insects and other habitats. As well as the fine morphological detail exhibited by the amber insect inclusions, various behaviours and interactions unlikely to be otherwise preserved can be found frozen in time, such as brooding behaviour and the entrapment of insects in spiders' webs. Insects in amber also provide important information about evolutionary changes over the course of the Cretaceous, including the rise of eusociality and angiosperm pollination.
... First, bird flowers have a more complex evolutionary history than fruits. A bird flower probably evolves from an ancestor pollinated by other animals with distinct colour visions in history (Kay & Grossenbacher, 2022;Wilson et al., 2007), as insect pollination evolved first in whole spermatophytes (Hu et al., 2008;Luo et al., 2018;Peris et al., 2017). Therefore, some flower traits adapting to other pollinators may be maintained in bird flowers and affect subsequent evolution (Thomson & Wilson, 2008;van der Niet & Johnson, 2012). ...
Pollination and seed dispersal are crucial processes for plant reproduction, sharing ecological relevance and similarities, yet they have rarely been considered together. Flowers appear to express greater phenotypic diversity than fruits due to multiple confounding factors, which pose challenges for comparative analyses. The colours of flowers and fruits are important visual signal traits in pollination and seed dispersal, evolving under different selective pressures from their respective pollinators and seed dispersers. Birds constitute a unique plant‐interacting group that participates in both pollination and seed dispersal events. In this study, we focus on red flowers and red fruits associated with avian mutualists to gain insight into the intrinsic differences between flowers/pollination and fruits/seed dispersal.
We conducted comparisons of colouration between 94 red flowers pollinated by birds and 99 red fruits dispersed by birds. The colour diversity was compared in both the spectral space and the avian colour vision spaces. Colour conspicuousness was analysed using avian colour vision models, as well as bee models. Pigeon colour preference was tested by controlled experiments utilizing red stimuli with and without secondary peaks at short wavelengths.
Red fruits had lower colour diversity than red flowers, with redder hues and fewer secondary reflectance peaks. Avian colour vision models illustrated that fruits were more conspicuous than flowers achromatically, but not chromatically. Pigeons did not show preference for red with or without a secondary peak.
Although both are red, there are significant differences between flowers and fruits in terms of colour diversity, spectral properties and colour perceptions. As we exclusively considered avian mutualists, these differences cannot be attributed to the differences in interacting animal groups or to their colour vision properties. This implies that the differences in evolutionary history between flowers and fruits may deserve further attention to understand the colour evolution.
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... Evidence suggests that early angiosperms were likely pollinated by beetles, given their ancient association and the relatively simple morphology of the earliest flowers [15]. As flowering plants diversified, offering varied floral forms, rewards, and scents, they paved the way for the evolution of more specialized pollinators like bees and butterflies. ...
Pollinators, particularly insects, play an indispensable role in ensuring the health of terrestrial ecosystems and in bolstering agricultural productivity. Their symbiotic relationship with plants has evolved over millennia, resulting in co-adaptations that facilitate the reproductive success of many plant species. This review sheds light on the multifaceted interactions between insect pollinators and plants, emphasizing their contributions not only in crop production but also in maintaining broader ecosystem services. The importance of insect pollinators, such as bees, butterflies, beetles, and flies, among others, is highlighted by their direct influence on the yield and quality of many crops. Notably, global agricultural sectors like fruits (e.g., apples and berries) and nuts (e.g., almonds) heavily depend on these insects for pollination. In economic terms, pollinators contribute substantially, with their decline potentially resulting in significant economic losses globally. Beyond agriculture, insect pollinators play a role in numerous ecosystem services. They aid in seed dispersal, ensuring gene flow and maintaining genetic diversity within plant populations. They act as crucial nodes in the food web, serving as prey for a plethora of species. They also indirectly support soil health by promoting the decomposition of plant matter, which enriches soil fertility and structure. Despite their importance, pollinators are under threat from various anthropogenic factors. Pesticides, habitat destruction, and climate change have been identified as primary drivers behind the decline of many pollinator species. Disease outbreaks and the proliferation of parasites further compound these challenges. Addressing these threats requires integrated conservation strategies. Practices like integrated pest management can minimize pesticide impact, while creating and maintaining pollinator habitats in agricultural and urban landscapes can provide refuges for these insects. Breeding programs targeting disease and parasite resistance and global collaborative efforts can further bolster pollinator populations. Investing in their conservation is not just an ecological imperative but also a socioeconomic one, ensuring food security for the growing global population. Emerging research avenues, such as genomic studies on pollinators, offer potential solutions and deeper insights into their resilience and adaptability. As the world grapples with escalating environmental challenges, understanding and supporting insect pollinators is paramount for a sustainable future.Insect pollinators
... Arguments supporting this come from extant and fossil flower morphology, fossilized traces of interactions, and the pollination modes of surviving early lineages. First, some extinct gymnosperms had bisporangiate cones (with both micro-and megasporangia) surrounded by bracts (Fig. 1), and many such cones show traces of having been chewed by mandibulate insects (Peris et al., 2017). Fossils of flower-associated flies also provide evidence of the existence of strobilus/pollinator interactions from the Permian to the Jurassic (Ren, 1998;Ren et al., 2009;Khramov et al., 2023). ...
This article is a Commentary on Stephens et al. (2023), 240: 880–891.
... In this relation, we could not verify pollen feeding based on preserved gut content in the fossils, suggesting that the beetles visited Ludwigia flowers not for pollen but for nectar. Flower visitation related to nectar and/or pollen feeding and/or pollination in various plant groups (at family, genus, or species level) is known to have changed and/or shifted between insect and/or other animal groups through geological time (e.g., Willmer, 2011;Orford et al., 2015;Peris et al., 2017;Dellinger et al., 2019;Wedmann et al., 2021;Gao et al., 2022). Therefore, we hypothesize that beetles were the main flower visitors and pollinators of European Ludwigia during the middle Eocene and that there has been a shift in primary flower visitors/pollinators, from beetles to bees, sometime during the late Paleogene to Neogene. ...
Paleogene flower-insect interactions and paleo-pollination processes are, in general, poorly understood and fossil evidence for such floral and faunal interactions are rarely reported. To shed light on angiosperm flower-insect interactions, we investigated several hundred fossil flowers and insects from the middle Eocene Fossil Lagerstätte of Eckfeld, Germany. During our work, we discovered a unique fossil Ludwigia flower (bud) with in situ pollen. The ecological preferences (climate, biome, habitat, etc.) of extant Ludwigia and the paleoecological configurations of the fossil plant assemblage support the taxonomic affiliation of the flower bud and an Eocene presence of Ludwigia in the vicinity of the former Lake Eckfeld. Today's Ludwigia are mostly pollinated by Hymenoptera (bees). Therefore, we screened all currently known hymenopteran fossils from Eckfeld but found no Ludwigia pollen adhering to any of the specimens. On the contrary, we discovered Ludwigia pollen adhering to two different groups of Coleoptera (beetles). Our study suggests that during the Eocene of Europe, Ludwigia flowers were visited and probably pollinated by beetles and over time there was a shift in primary flower visitors/pollinators, from beetles to bees, sometime during the late Paleogene to Neogene.
... When flowering plants (Angiospermae) rose to prominence in the mid-Cretaceous (~ 100 million years ago), the relationship between insects and flowers was already ancient (Peris et al. 2017, Ollerton 2017. The key innovation of angiosperms was not that they bore flowers, for the homologous flowers sensu lato of gymnosperms not only existed but were already associated with insect pollinators when angiosperms arose (Frame 2003, Peris et al. 2017. ...
... When flowering plants (Angiospermae) rose to prominence in the mid-Cretaceous (~ 100 million years ago), the relationship between insects and flowers was already ancient (Peris et al. 2017, Ollerton 2017. The key innovation of angiosperms was not that they bore flowers, for the homologous flowers sensu lato of gymnosperms not only existed but were already associated with insect pollinators when angiosperms arose (Frame 2003, Peris et al. 2017. Rather, it was their edibility, and especially that of their flowers, that distinguished angiosperms from their predecessors and paved the way for their rapid co-diversification with pollinating insects (Frame 2003). ...
The mutualism between plants and pollinators is built upon the trophic ecology of flowers and florivores. Yet the ecology of flowers‐as‐food is left implicit in most studies of plant–pollinator ecology, and it has been largely neglected in mainstream trophic ecology. This deficit is especially evident in an emerging issue of basic and applied significance: competition between pollinators for floral resources. In this synthesis, we start by exploring the notion of floral resource limitation upon which most studies concerning competition between pollinators are tacitly predicated. Both theoretical and empirical lines of evidence indicate that floral resource limitation must be understood as a complex ecological contingency; the question is not simply whether but when, where and in what regions of floral trait space resources are limiting. Based on this premise, we propose a framework for understanding floral resource availability in terms of temporal, spatial and functional structure. While this framework is conceptually intuitive, it is empirically and analytically demanding. We review existing methods for measuring and summarizing the multi‐dimensional structure of floral resources, highlight their strengths and weaknesses, and identify opportunities for future methods development. We then discuss the causal relationships linking floral resource structure to species coexistence, plant–pollinator community dynamics, and exogenous drivers like climate, land use, and episodic disturbances. In its role as both cause and effect, floral resource structure mediates the relationship between behavioral ecology, landscape ecology, and coexistence theory with respect to flowers and florivores. Establishing floral resource structure as an object of study and application will both shed light on basic questions of coexistence and guide management decisions concerning contentious issues such as the compatibility of apiculture with wild pollinator conservation and the appropriate use of floral enhancements in agri‐environment schemes.
... During this time, the Mesophytic paleobiome dominated by "gymnosperms" was replaced by a Cenophytic paleobiome dominated by angiosperms (Labandeira, 2014b;McElwain, 2018;Birks, 2020;Condamine et al., 2020). This turnover altered the base of trophic networks within continental ecosystems (Labandeira, 2014b), substantially modifying communities of herbivores (Labandeira, 2007;Kergoat et al., 2014) and, therefore, affecting the composition and evolution of continental biotas (Meredith et al., 2011;McKenna et al., 2015;Peris et al., 2017;Benson et al., 2021;Peris and Condamine, 2023). ...
... Angiosperm resin terpenoids attract insect pollinators (Armbruster, 1984;Boncan et al., 2020). Highly specialized pollination relationships between some groups of insects and "gymnosperms" have been discovered in amber since the Albian (Fig. 5C), in some instances lacking extant representatives of such pollination interactions (Peñalver et al., , 2015Peris et al., 2017Peña-Kairath et al., 2023). Resin exudation by conifers during the CREI could be related to the attraction of certain groups of insects to assist in pollination. ...
THE PAPER IS IN OPEN ACCESS IN THE URL:
https://doi.org/10.1016/j.earscirev.2023.104486
Amber is fossilized resin that preserves biological remains in exceptional detail, study of which has revolutionized understanding of past terrestrial organisms and habitats from the Early Cretaceous to the present day. Cretaceous amber outcrops are more abundant in the Northern Hemisphere and during an interval of about 54 million years, from the Barremian to the Campanian. The extensive resin production that generated this remarkable amber record may be attributed to the biology of coniferous resin producers, the growth of resiniferous forests in proximity to transitional sedimentary environments, and the dynamics of climate during the Cretaceous. Here we discuss the set of interrelated abiotic and biotic factors potentially involved in resin production during that time. We name this period of mass resin production by conifers during the late Mesozoic, fundamental as an archive of terrestrial life, the ‘Cretaceous Resinous Interval’ (CREI).
