Different Solanum species
Cultivated tomatoes, Solanum lycopersicum
New tomato, potato family tree shows that fruit color and size evolved together | Penn State University
The Solanaceae is a large family of plants which includes potatoes, tomatoes, aubergines and peppers/capsicums, and some highly poisonous plants such as deadly nightshade and thornapple. Some of them are economically and nutritionally important food crops.
A feature of the family is the high level of toxicity of most parts of the plants, even important crops like potatoes, all parts of which, apart from the tubers, are highly poisonous, even the small green tomato-like fruits. Similarly, all parts of the closely related tomato plant, apart from the fruits, are highly toxic.
What can you tell me about the Solanaceae and the time-scale of their evolution?
The Solanaceae, commonly known as the nightshade family, is a diverse and economically significant family of flowering plants. This family includes well-known species such as tomatoes, potatoes, eggplants, bell peppers, and tobacco. Understanding the evolution and diversification of the Solanaceae involves looking at their origin, diversification events, and the adaptive radiation that led to the variety of species we see today.
Evolutionary Origin and Timeline
- Early Origins: The Solanaceae family is believed to have originated during the late Cretaceous period, around 80-90 million years ago (mya). This timing is based on molecular clock estimates and fossil records.
- Diversification: Significant diversification within the family occurred during the Paleocene and Eocene epochs (about 66-34 mya), likely driven by climatic changes and the availability of new ecological niches.
Key Evolutionary Events
- Initial Diversification: The early diversification of Solanaceae likely took place in South America, which is considered the primary center of origin for the family. The varied climates and geographies of this region provided multiple ecological niches.
- Dispersal and Adaptation: As members of the Solanaceae spread to different parts of the world, they adapted to a wide range of environments. This includes the arid regions of Australia and the temperate climates of North America and Europe.
- Radiation of Major Genera: Key genera within the family, such as Solanum (which includes tomatoes and potatoes), diversified significantly during the Miocene epoch (23-5 mya). This period was marked by further climatic changes that created new habitats.
Morphological and Genetic Diversification
- Morphological Adaptations: Solanaceae species exhibit a wide range of growth forms, from herbaceous plants to shrubs and small trees. They have also developed various fruit types, including berries, capsules, and drupes.
- Genetic Studies: Advances in molecular genetics have provided insights into the evolutionary relationships within the family. Phylogenetic studies based on DNA sequencing have helped clarify the lineage and divergence times of different genera and species.
Ecological and Economic Importance
- Agricultural Significance: Many Solanaceae species are essential crops with significant agricultural value. Tomatoes, potatoes, and peppers are staple foods in many cultures.
- Medicinal and Toxic Properties: Some members of the Solanaceae family produce alkaloids that have medicinal properties, such as atropine and scopolamine, used in various treatments. However, some species are also toxic and have been used historically as poisons.
Evolutionary Challenges and Research Directions
- Hybridization and Polyploidy: Hybridization and polyploidy (having multiple sets of chromosomes) have played a role in the evolution of some Solanaceae species, contributing to their genetic diversity.
- Conservation and Study: Preserving the genetic diversity of wild Solanaceae species is important for both conservation and potential agricultural benefits. Continued research on their genetics and evolutionary history can provide valuable insights into plant evolution and adaptation.
In summary, the Solanaceae family has a rich evolutionary history that spans tens of millions of years. Its members have adapted to a wide range of ecological niches, leading to the diverse array of species we see today. This evolutionary journey has been shaped by climatic changes, geographical dispersal, and genetic diversification.
Which species are the result of hybridization and/or polyploidy?
Hybridization and polyploidy have played significant roles in the evolution of many species within the Solanaceae family. Here are some notable examples:
Hybridization
Hybridization has contributed to the genetic diversity and speciation within the Solanaceae family. Some examples include:
- Tomato (Solanum lycopersicum):
- The cultivated tomato (Solanum lycopersicum) has undergone hybridization with wild relatives, leading to the development of various cultivars with different desirable traits such as disease resistance, fruit size, and flavor.
- Wild species such as Solanum pimpinellifolium and Solanum cheesmaniae have contributed genetic material to cultivated tomatoes through both natural hybridization and intentional breeding.
- Potato (Solanum tuberosum):
- The cultivated potato (Solanum tuberosum) is a complex hybrid species. It has hybridized with various wild potato species, such as Solanum demissum and Solanum acaule, which have contributed to its genetic makeup and provided resistance to diseases like late blight.
- Pepper (Capsicum species):
- Hybridization among different Capsicum species has been common in the cultivation of peppers. For instance, Capsicum annuum (bell pepper, chili pepper) has hybridized with other species such as Capsicum frutescens and Capsicum chinense to produce new varieties with different heat levels and flavors.
Polyploidy
Polyploidy has been an important mechanism in the evolution of certain Solanaceae species. Polyploid species often exhibit greater genetic diversity and adaptability.
- Potato (Solanum tuberosum):
- The cultivated potato is a tetraploid species (4 sets of chromosomes, 2n = 4x = 48), resulting from the polyploidization of diploid ancestors. This polyploid nature has contributed to its genetic complexity and adaptability.
- Tobacco (Nicotiana tabacum):
- Nicotiana tabacum, the species used for commercial tobacco, is an allotetraploid (4 sets of chromosomes, 2n = 4x = 48). It originated from the hybridization of two diploid species, Nicotiana sylvestris and Nicotiana tomentosiformis, followed by chromosome doubling.
- Wild Potatoes:
- Several wild potato species are polyploids. For example, Solanum demissum is a hexaploid species (6 sets of chromosomes, 2n = 6x = 72), and it has been used in breeding programs to introduce disease resistance genes into cultivated potatoes.
Importance of Hybridization and Polyploidy
Genetic Diversity: Both hybridization and polyploidy contribute to genetic diversity, providing a broader range of traits that can be selected for in breeding programs.
Adaptability: Polyploid species often have greater genetic variability, which can enhance their adaptability to different environmental conditions and stresses.
Crop Improvement: Understanding the genetic contributions from hybridization and polyploidy is crucial for crop improvement efforts, allowing for the development of new varieties with desirable traits such as increased yield, disease resistance, and improved nutritional content.
Overall, hybridization and polyploidy have been vital in shaping the evolution and diversity of the Solanaceae family, leading to the development of many economically important species and cultivars.
Now researchers at Penn State University, have produced a new evolutionary tree of the family which explains how the fruits of the plants evolved their size and colour together and that fruit-eating animals were probably not the main drivers of their evolution, as was previously thought.
The team have just
published their findings, open access, in the journal
New Phytologist. It is explained in the press release from Penn State:
Fruits of Solanum plants, a group in the nightshade family, are incredibly diverse, ranging from sizable red tomatoes and purple eggplants to the poisonous green berries on potato plants. A new and improved family tree of this group, produced by an international team led by researchers at Penn State, helps explain the striking diversity of fruit colors and sizes and how they might have evolved.
The team found that the size and color of fruits evolved together and that fruit-eating animals were like not the primary drivers of the fruits’ evolution, as had been previously thought. The study, published in the journal New Phytologist, may also provide insight into breeding agriculturally important plants with more desirable traits, the researchers said.
“There are about 1,300 species in the genus Solanum, making it one of the most diverse plant genera in the world,” said João Vitor Messeder, graduate student in ecology and biology in the Penn State Eberly College of Science and Huck Institutes for the Life Sciences and lead author of the paper. “Since the 1970s and ‘80s, researchers have suggested that birds, bats and other fruit-eating animals have driven the evolution of fruits like those in Solanum. However, the importance of the evolutionary history of the plants has been underestimated or rarely considered when evaluating the diversification of fleshy fruits. To better test this hypothesis, we needed first to produce a more robust phylogeny, or family tree, of this plant group to improve our understanding of the relationships between species.”
Plants in the genus Solanum produce fruits with a wide variety of sizes, colors and nutritional values. They can appear black, purple, red, green, yellow or orange and range in size from less than a quarter of an inch to as much as 8 inches, or 0.5 to 20 centimeters. In addition to agriculturally important plants, some plants in the group are cultivated for their ornamental flowers, and the fruits of many of these plants are eaten by humans and a large diversity of animals, including birds, bats, reptiles, primates and other land mammals.
The researchers collected samples of plants from across the world, including wild plants from Brazil, Peru and Puerto Rico and plants from botanical gardens, and sequenced their genes from RNA. They supplemented with previously collected samples and publicly available data, ultimately comparing the sequences of 1,786 genes from a total of 247 species to reconstruct the Solanum family tree. This included representatives from all 10 of the major clades — the branches of the tree — and 39 of 47 minor clades within the genus.
“By using thousands of genes shared among species that effectively represented the entire genus, we significantly improved the Solanum family tree, making it the most comprehensive to date,” said Messeder, who conducted the research in the lab of Hong Ma, Huck Chair in Plant Reproductive Development and Evolution and professor of biology at Penn State and a co-corresponding author of the paper. “Recent advances in technology allowed us to use more genes than previous studies, which faced many challenges in resolving relationships between species and clades. This improved tree helps us understand when different fruit colors and sizes originated or how they changed as new plant species came about.”
The researchers added considerable resolution of the smaller branches in the group that includes potatoes and tomatoes, as well as their closely and more distantly related wild species. The insights gained, the researchers said, could support crop improvement programs for these species and other crops in the genus.
“If the closest wild relatives of important agricultural crops have desirable traits, it is possible to breed crops with those species or borrow their genes, for example to improve resistance to temperature or pests or to produce larger fruits or fruits of a certain color,” Messeder said.
The researchers found that the color and size of Solanum fruits was fairly conserved over evolutionary history, meaning that closely related species tend to have similar fruits. The evolution of fruit color and size is also correlated, with changes in one trait often corresponding to changes in the other, leading fruits of certain colors to be bigger than fruits of other colors.
“These results suggest that physiological and molecular mechanisms may play a role in keeping the evolution of fruit color and size tied together,” Messeder said. “While frugivores — or animals that primarily eat fruit — and seed dispersers may influence diversification, we need to consider all of the possibilities when studying how fruits became so diverse.”
The researchers also clarified the origin and diversification timeline of this genus, in part by including recent information from the oldest nightshade family fossil — from a different genus in the Nightshade family whose fossil was dated to about 52 million years ago — and from particular genes that improved estimates of the length of evolutionary branches. The researchers dated the origin of Solanum to about 53.1 million years ago — a full 30 million years earlier than prior estimates that were based on genes from other parts of the plant cell. This paints a new picture of the environment that might have shaped how these plants diversified into new groups and species.
“The Earth’s environment changed dramatically during the 30 million years in terms of temperature, carbon dioxide in the atmosphere, geography and animal diversity,” Messeder said. “Now that we know when Solanum and its subgroups originated, we can think about the conditions that might have promoted the diversification of that group, as well as how other organisms might have played a role.”
The team found that the earliest members of Solanum had medium-sized berries that remained green when ripe, and that green and yellow fruits of this group became more diverse around 14 million years ago. The researchers speculated that bats might have played a role in this diversification, given their similar evolutionary timeline and that they are the primary dispersers of modern green and yellow Solanum fruits. As new bat species arose and expanded where they were living during this time, they ate Solanum fruits and carried their seeds to new environments.
Next, the researchers plan to explore how modern interactions between animals and the fruit they eat may shed light on the evolution of both groups as well as explore the evolution of certain genes relevant to fruit color and size.
In addition to Messeder and Ma, the research team includes Tomás Carlo, professor of biology at Penn State; Guojin Zhang, postdoctoral researcher at Penn State at the time of the research; Juan David Tovar at the National Institute of Amazonian Research in Brazil; César Arana at the National University of San Marcos in Peru; and Jie Huang and Chien-Hsun Huang at Fudan University in China.
Summary
- Mutualisms between plants and fruit-eating animals were key to the radiation of angiosperms. Still, phylogenetic uncertainties limit our understanding of fleshy-fruit evolution, as in the case of Solanum, a genus with remarkable fleshy-fruit diversity, but with unresolved phylogenetic relationships.
- We used 1786 nuclear genes from 247 species, including 122 newly generated transcriptomes/genomes, to reconstruct the Solanum phylogeny and examine the tempo and mode of the evolution of fruit color and size.
- Our analysis resolved the backbone phylogeny of Solanum, providing high support for its clades. Our results pushed back the origin of Solanum to 53.1 million years ago (Ma), with most major clades diverging between 35 and 27 Ma. Evolution of Solanum fruit color and size revealed high levels of trait conservatism, where medium-sized berries that remain green when ripe are the likely ancestral form. Our analyses revealed that fruit size and color are evolutionary correlated, where dull-colored fruits are two times larger than black/purple and red fruits.
- We conclude that the strong phylogenetic conservatism shown in the color and size of Solanum fruits could limit the influences of fruit-eating animals on fleshy-fruit evolution. Our findings highlight the importance of phylogenetic constraints on the diversification of fleshy-fruit functional traits.
Introduction
The fleshy fruits of angiosperms are key innovations that mediate mutualistic seed dispersal by fruit-eating animals (i.e. frugivores) (Eriksson, 2016). This plant–animal interdependence is central to the development and organization of terrestrial communities (Bascompte & Jordano, 2007; Fleming & Kress, 2013). By encapsulating seeds within nutritious pulp, plants take advantage of foraging animals to effectively disseminate their seeds (Schupp et al., 2010). Thus, frugivores can increase plant fitness, and drive the evolution of fruit types (e.g. fleshy fruits) and fleshy-fruit traits (e.g. color) (Lomáscolo et al., 2010.1; Eriksson, 2016; Xiang et al., 2024). Still, it remains unclear how shared evolutionary history influences the evolution of the functional traits of fleshy fruits among related species. Specifically, to examine how frugivores may affect the evolution of fruit traits, it is crucial to assess whether a trait is conserved and has evolved a few or multiple times within a lineage (Ackerly, 2009).
Differences in fruit traits such as size and color when ripe have been interpreted as adaptations to different types of frugivores (Van Der Pijl, 1982; Valenta & Nevo, 2020). For example, birds typically feed on small brightly colored fruits given their highly developed color vision and narrow bill gapes (Janson, 1983; Wheelwright, 1985; Wheelwright & Janson, 1985.1). In comparison with birds, mammals have more limited color vision but highly developed olfaction, teeth, and forelimbs that aid in the manipulation and use of fruits that are large, tough, dull-colored, and odoriferous (Janson, 1983; Nevo et al., 2018). Such trait-matching suggests that frugivores could drive the evolution of fruit traits through natural selection (i.e. dispersal syndrome hypothesis) (Van Der Pijl, 1982; Janson, 1983; Valenta & Nevo, 2020). For instance, fruit traits of figs (Ficus spp., Moraceae) converge to small brightly colored fruits when birds are the main frugivores, or to larger dull-colored fruits when bats and other mammals are the main frugivores (Lomáscolo et al., 2008, 2010.1). Similarly, other phylogenetic comparative studies have also suggested that frugivores are the main drivers shaping fruit characteristics that lead to general ‘syndromes’ that match distinct frugivore groups (Valenta et al., 2018.1; Nevo et al., 2018; do Nascimento et al., 2020.1; Barnett et al., 2023a,2023.1b). It is expected that when selective pressures from frugivores are convergent, the characteristics of fleshy fruits might be less predictable by phylogenetic relationships (Ackerly, 2009; Valenta & Nevo, 2020).
Although the dispersal syndrome hypothesis offers a compelling explanation for fruit trait diversity rooted in selection theory and adaptation, the evidence remains inconclusive (Valenta & Nevo, 2020). This is because many plant species can be effectively dispersed by animals with distinct morphologies and physiologies, leading to diffuse selective pressures that may preclude adaptation to specific frugivores (Herrera, 1985.2). Furthermore, fruit traits may be phylogenetically determined, limiting the selective pressures from frugivores on fruit trait evolution (Fischer & Chapman, 1993; Jordano, 1995; Ackerly, 2009). In such cases, trait matching is more likely the result of ecological fitting (i.e. pre-existing traits fitting new ecological niches without further modification) rather than the evolution of new traits due to selection (Janzen, 1985.3; Agosta & Klemens, 2008.1). Thus, how much fruit traits are the result of adaptations or of phylogenetic constraints and ecological fitting remains unclear. Advance in this field has been constrained by the use of limited phylogenetic frameworks, poorly resolved phylogenies, and additional challenges posed by hybridization and introgression events among species (e.g. Gardner et al., 2023.2).
Recent studies merging phylogenetics and trait evolution have provided important insights into fleshy-fruit evolution. Fleshy fruits have independently evolved multiple times across angiosperms (Xiang et al., 2017, 2024; Frost et al., 2021; Hilgenhof et al., 2023.3). Studies have shown that fruit color can be associated with long-distance dispersal patterns (Lu et al., 2019) and diversification rates (Spriggs et al., 2015; Lu et al., 2019; L. Zhang et al., 2023.4). Fruit developmental processes have been identified as a mechanism underlying the origin of syndromes (Sinnott-Armstrong et al., 2020.2). Still, in-depth studies assessing the role of shared evolutionary histories on fruit trait evolution remain scarce, especially within highly diverse plant groups.
The genus Solanum L. comprises c. 1300 fleshy-fruited species and is the largest genera of Solanaceae and the second largest genus of fleshy-fruited plants (Frodin, 2004). Regarding fruit traits, Solanum shows a remarkably high diversity, producing berries of various sizes, colors, and pulp with different nutritional and chemical profiles (Cipollini et al., 2002; Knapp et al., 2004.1; Hilgenhof et al., 2023.3). For instance, berry size ranges between 0.5 and 20.0 cm, ripening in many colors, including black, purple, red, green, yellow, and orange. Additionally, Solanum fruits with different colors and sizes are eaten and dispersed by distinct animal groups, including reptiles, birds, bats, primates, and terrestrial mammals (Symon, 1979; Cáceres & Moura, 2003; Arruda Bueno & Motta-Junior, 2004.2; Vasconcellos-Neto et al., 2009.1; Jacomassa & Pizo, 2010.2). This unusual fruit diversity within a single genus makes Solanum an excellent group to investigate a wide range of eco-evolutionary questions (Knapp et al., 2004.1; Moyle, 2008.2). Furthermore, humans have cultivated and domesticated many Solanum species, such as the potato (S. tuberosum), tomato (S. lycopersicum), eggplant (S. melongena), and others (S. betaceum, S. muricatum, and S. quitoense), contributing to the global agriculture (Knapp et al., 2004.1). However, uncertainties in the phylogeny of Solanum limit our understanding of the evolution and diversification patterns of fruit traits relevant to plant–frugivore interactions and agriculture. Unclear phylogenetic relationships make it challenging to determine the ancestral form of a trait and track the number of times and the direction of transitions of the fruit trait over time. Furthermore, assessing the lability of a trait may facilitate its manipulation for agriculture.
Previous studies have made significant progress toward reconstructing the evolutionary history of Solanum (Weese & Bohs, 2007.1; Särkinen et al., 2013.1; Gagnon et al., 2022; Huang et al., 2023.5), with the identification of three deep lineages (we adopted the informal clade nomenclature proposed in previous molecular phylogenetic studies – Bohs, 2005; Stern et al., 2011; Särkinen et al., 2013.1; Tepe et al., 2016.1; Gagnon et al., 2022). The Thelopodium Clade, comprising three species, diverges first, while the remaining species are divided into Clades I and II. Clade I contains c. 350 species, including tomato and potato, whereas Clade II, with c. 900 species, has many spiny shrubs, including eggplant. Clades I and II were further subdivided into nine major and 47 minor clades (Särkinen et al., 2013.1). However, the placement of many clades is inconsistent among studies using various taxa and genes (Särkinen et al., 2013.1; Gagnon et al., 2022; Huang et al., 2023.5) (Supporting Information Fig. S1). Recently, a comprehensive phylogenetic study of 742 Solanum species still found major clades with unresolved relationships (Fig. S1) (Gagnon et al., 2022). For example, the monophyly of Clade I was supported by some analyses using plastid sequences (Fig. S1a–c) but not others using nuclear genes (Fig. S1d,e), and placement of its major clades – especially Regmandra – was uncertain (Fig. S1c–e). These inconsistencies have been described as polytomies near the crown node and reflect difficulties for resolving the deep Solanum relationships (Gagnon et al., 2022). Another recent study (Huang et al., 2023.5) using 1699 genes from 81 Solanum species, along with other members of Solanaceae, presented a well-supported phylogeny, but lacked the Thelopodium Clade and some major clades in Clades I and II, including Regmandra (Fig. S1f–k) and many minor clades. Consequently, a Solanum phylogeny with a more complete lineage representation and well-supported relationships is needed to further understand the ecological factors that shape its evolution, including the drivers behind its remarkable diversity of fruit sizes, shapes, and colors.
Here, we bridge the gap between ecology and phylogenomics using Solanum as study group to examine the tempo and mode of the evolution of fruit traits that are both agriculturally relevant and mediate frugivory and seed dispersal interactions. We used 1786 low-copy nuclear genes across 247 species to reconstruct a highly resolved Solanum phylogeny. We explored the temporal aspects of Solanum's evolutionary history and investigated the phylogenetic effects on the diversification patterns of two important fruit functional traits: size and color when ripe. We evaluated how evolutionarily constrained are fruit size and color in Solanum and discussed implications for the ecology and evolution of seed dispersal mutualisms.
Fig. 2
Divergence time estimation for
Solanum indicating its origin in early Eocene and divergence among extant species starting in the middle Eocene. Relevant estimated divergence times of major clade lineages are marked at corresponding nodes. Branch colors match major clade colors of Fig.
1, with their respective names on the right side. Fruit colors and sizes are mapped on terminal tips. At the bottom of the chronogram, geological timescale is shown with periods delimited by vertical lines, the estimated temperature variation for the Cenozoic, and arrows indicating the Mid-Eocene Climatic Optimum and Mid-Miocene Climatic Optimum. Eo, Eocene; LC, late Cretaceous; Mio, Miocene; Ol, Oligocene; Pal, Paleocene; Pli, Pliocene; Q, Quaternary. On the right side, pictures demonstrate some of the variety of colors, sizes, and shapes that can be found in
Solanum fruits. Pictures were taken by the authors or downloaded from the internet (Supporting Information Table
S6). (Detailed divergence times with species names are shown in Figs
S6,
S7).
Messeder, J.V.S., Carlo, T.A., Zhang, G., Tovar, J.D., Arana, C., Huang, J., Huang, C.-H. and Ma, H. (2024)
A highly resolved nuclear phylogeny uncovers strong phylogenetic conservatism and correlated evolution of fruit color and size in Solanum L..
New Phytol, 243: 765-780. https://doi.org/10.1111/nph.19849
Copyright: © 2024 The authors.
Published by John Wiley & Sons. Open access.
Reprinted under a
Creative Commons Attribution 4.0 International license (CC BY 4.0)
Of special concern for creationists, is not the technical details, which few would understand even if they read it, but the timeline and the fact that the scientists show no hint of giving up on the Theory of Evolution but instead, use it to explain their findings, with no hint that a magic supernatural entity intervened anywhere in the divergence process.
Additionally, the Introduction section contains links to lots of references to papers dealing with the same or related subjects. None of them show any signs of adopting creationism because the TOE isn't up to the task, either.
The entire range of
Solanum species, including many important foods, is the result of evolution, with new genetic information being created by the natural processes of gene and whole genome duplication to give polyploidy, and hybridization. The potatoes, tomatoes, peppers, chilis and aubergines we eat contain evidence of evolution in their genomes.
Many of these plants are the product of cultivation and human selective breeding of course, so creationists might like to explain why plants, like domestic animals, which are the descendants of species the Bible says were created for humankind, have had to be improved to make them fit for purpose. Did their designer not know what humans would need, or did the authors of the Bible not understand about domestication, cultivation and selective breeding to improve on the wild type?
