Guillaume Chomicki | The University of Sheffield (original) (raw)

Papers by Guillaume Chomicki

Research paper thumbnail of World list ant plants 22 06 19 UPDATED

https://guillaumechomicki.wixsite.com/mysite/lab-resources, 2019

The world list of plant with ant domatia -- UPDATED

Research paper thumbnail of Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

eLife, Oct 27, 2022

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense deb... more The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined towards the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with past climate changes. Editor's evaluation This important work by Meseguer et al. depicts findings that substantially advance our understanding of clade diversification across major Neotropical bioregions. The evidence that summarises the evolutionary diversity dynamics of 150 time-calibrated clades of neotropical plants and animals data is convincingly presented with current state-of-the-art analyses. The work will be of interest to evolutionary biologists and biogeographers working to understand the origins of the most biodiverse land mass on the planet.

Research paper thumbnail of Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Zenodo (CERN European Organization for Nuclear Research), Jul 11, 2021

The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto r... more The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto relied heavily on plastid DNA sequences and limited taxon sampling. Previous studies have provided a robust plastid phylogenetic framework, which was used to classify orchids and investigate the drivers of orchid diversification. However, the extent to which phylogenetic inference based on the plastid genome is congruent with the nuclear genome has been only poorly assessed. METHODS: We inferred higher-level phylogenetic relationships of orchids based on likelihood and ASTRAL analyses of 294 low-copy nuclear genes sequenced using the Angiosperms353 universal probe set for 75 species (representing 69 genera, 16 tribes, 24 subtribes) and a concatenated analysis of 78 plastid genes for 264 species (117 genera, 18 tribes, 28 subtribes). We compared phylogenetic informativeness and support for the nuclear and plastid phylogenetic hypotheses. RESULTS: Phylogenetic inference using nuclear data sets provides well-supported orchid relationships that are highly congruent between analyses. Comparisons of nuclear gene trees and a plastid supermatrix tree showed that the trees are mostly congruent, but revealed instances of strongly supported phylogenetic incongruence in both shallow and deep time. The phylogenetic informativeness of individual Angiosperms353 genes is in general better than that of most plastid genes. CONCLUSIONS: Our study provides the first robust nuclear phylogenomic framework for Orchidaceae and an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely thoroughly documented: nuclear and plastid phylogenetic trees can contain strongly supported discordances, and this incongruence must be reconciled prior to interpretation in evolutionary studies, such as taxonomy, biogeography, and character evolution.

Research paper thumbnail of Chromosome numbers, Sudanese wild forms, and classification of the watermelon genus <i>Citrullus</i> , with 50 names allocated to seven biological species

Taxon, Nov 30, 2017

Watermelons are among the most important vegetable crops worldwide, but targeted breeding is hind... more Watermelons are among the most important vegetable crops worldwide, but targeted breeding is hindered by problems with Citrullus taxonomy. Here we clarify nomenclature and species relationships in Citrullus, its chromosome numbers, and the likely geographic region of watermelon domestication. We correct an erroneous chromosome count in recent literature, provide a count for an understudied species, and data on chromosome numbers for the entire genus. We also use a nuclear/ plastid locus phylogeny to summarize data on Citrullus sexual systems, loss of tendrils, life history, and geographic ranges. Key insights from new sequences are that (i) material of C. vulgaris var. "colocynthoides", collected by Schweinfurth in Egypt in 1882 represents the colocynth, C. colocynthis, and (ii) the citron or bitter watermelon, C. amarus, is indeed a separate species, not a subspecies of the dessert watermelon. Schweinfurth's varietal name, a nomen nudum, has been widely used for seeds as old as 5400 BP, and it now needs to be investigated whether these seeds are colocynths, watermelon or a hybrid. To help improve Citrullus taxonomy and nomenclature, we allocate some 50 scientific names to seven biological species, tabulate chromosome counts, and provide notes on misidentified germplasms traceable by accession numbers. More wildcollected herbarium-verified material from northeast Africa is urgently needed, especially given the discovery of Russian breeders that populations of wild "cordophanus" from Sudan are closer to the cultivated watermelon than are any other wild populations so far known.

Research paper thumbnail of Evolutionary Relationships and Biogeography of the Ant-Epiphytic Genus Squamellaria (Rubiaceae: Psychotrieae) and Their Taxonomic Implications

PLOS ONE, Mar 30, 2016

Ecological research on ant/plant symbioses in Fiji, combined with molecular phylogenetics, has br... more Ecological research on ant/plant symbioses in Fiji, combined with molecular phylogenetics, has brought to light four new species of Squamellaria in the subtribe Hydnophytinae of the Rubiaceae tribe Psychotrieae and revealed that four other species, previously in Hydnophytum, need to be transferred to Squamellaria. The diagnoses of the new species are based on morphological and DNA traits, with further insights from microCT scanning of flowers and leaf δ 13 C ratios (associated with Crassulacean acid metabolism). Our field and phylogenetic work results in a new circumscription of the genus Squamellaria, which now contains 12 species (to which we also provide a taxonomic key), not 3 as in the last revision. A clock-dated phylogeny and a model-testing biogeographic framework were used to infer the broader geographic history of rubiaceous ant plants in the Pacific, specifically the successive expansion of Squamellaria to Vanuatu, the Solomon Islands, and Fiji. The colonization of Vanuatu may have occurred from Fiji, when these islands were still in the same insular arc, while the colonization of the Solomon islands may have occurred after the separation of this island from the Fiji/Vanuatu arc. Some of these ant-housing epiphytes must have dispersed with their specialized ants, for instance attached to floating timber. Others acquired new ant symbionts on different islands.

Research paper thumbnail of The Origins and Drivers of Neotropical Diversity

bioRxiv (Cold Spring Harbor Laboratory), Feb 25, 2021

The origin of the outstanding Neotropical biodiversity is still debated. A comprehensive understa... more The origin of the outstanding Neotropical biodiversity is still debated. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here we define and evaluate four evolutionary scenarios assuming different diversity trajectories and drivers of Neotropical diversification. Relying on 150 phylogenies (12,512 species) of seed plants and tetrapods, we found that diversity mostly expanded through time (70% of the clades), but scenarios of saturated (21%) and declining (9%) diversity also account for a substantial proportion of Neotropical diversity. These scenarios occur indistinctly across the major regions, habitats, and altitudes of the Neotropics, suggesting no geographic structure of Neotropical diversification. On the contrary, diversification dynamics differ across taxonomic groups: plant diversity mostly expanded through time (88%), while for a significant fraction of tetrapods (43%) diversity accumulated at a slower pace or declined toward the present. These opposite evolutionary patterns reflect different capacities for plants and tetrapods to cope with environmental change, especially in relation to climate cooling. Our results suggest that the assembly of Neotropical diversity is a long, clade-specific, and complex process resulting from a combination of gradual and pulse dynamics associated with environmental stability and instability over macroevolutionary scales. .

Research paper thumbnail of Author response: Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

Research paper thumbnail of Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

eLife

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense deb... more The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In ...

Research paper thumbnail of Genome Sequencing of up to 6,000-Year-OldCitrullusSeeds Reveals Use of a Bitter-Fleshed Species Prior to Watermelon Domestication

Molecular Biology and Evolution

Iconographic evidence from Egypt suggests that watermelon pulp was consumed there as a dessert by... more Iconographic evidence from Egypt suggests that watermelon pulp was consumed there as a dessert by 4,360 BP. Earlier archaeobotanical evidence comes from seeds from Neolithic settlements in Libya, but whether these were watermelons with sweet pulp or other forms is unknown. We generated genome sequences from 6,000- and 3,300-year-old seeds from Libya and Sudan, and from worldwide herbarium collections made between 1824 and 2019, and analyzed these data together with resequenced genomes from important germplasm collections for a total of 131 accessions. Phylogenomic and population-genomic analyses reveal that (1) much of the nuclear genome of both ancient seeds is traceable to West African seed-use “egusi-type” watermelon (Citrullus mucosospermus) rather than domesticated pulp-use watermelon (Citrullus lanatus ssp. vulgaris); (2) the 6,000-year-old watermelon likely had bitter pulp and greenish-white flesh as today found in C. mucosospermus, given alleles in the bitterness regulators ...

Research paper thumbnail of A highly contiguous, scaffold-level nuclear genome assembly for the Fever tree (Cinchona pubescens Vahl) as a novel resource for research in the Rubiaceae

BackgroundThe Andean Fever tree (Cinchona L.; Rubiaceae) is the iconic source of bioactive quinin... more BackgroundThe Andean Fever tree (Cinchona L.; Rubiaceae) is the iconic source of bioactive quinine alkaloids, which have been vital to treating malaria for centuries. C. pubescens Vahl, in particular, has been an essential source of income for several countries within its native range in north-western South America. However, an absence of available genomic resources is essential for placing the Cinchona species within the tree of life and setting the foundation for exploring the evolution and biosynthesis of quinine alkaloids.FindingsWe address this gap by providing the first highly contiguous and annotated nuclear and organelle genome assemblies for C. pubescens. Using a combination of ∼120 Gb of long sequencing reads derived from the Oxford Nanopore PromethION platform and 142 Gb of short-read Illumina data. Our nuclear genome assembly comprises 603 scaffolds comprising a total length of 904 Mb, and the completeness represents ∼85% of the genome size (1.1 Gb/1C). This draft genome...

Research paper thumbnail of Data from: Experimental signal dissection and method sensitivity analyses reaffirm the potential of fossils and morphology in the resolution of the relationship of angiosperms and Gnetales

The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmat... more The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmatic problems in plant evolution, with morphological analyses (which have usually included fossils) and molecular analyses pointing to very distinct topologies. Almost all morphology-based phylogenies group angiosperms with Gnetales and certain extinct seed plant lineages, while most molecular phylogenies link Gnetales with conifers. In this study, we investigate the phylogenetic signal present in published seed plant morphological datasets. We use parsimony, Bayesian inference, and maximum likelihood approaches, combined with a number of experiments with the data, to address the morphological-molecular conflict. First, we ask whether the lack of association of Gnetales with conifers in morphological analyses is due to an absence of signal or to the presence of competing signals, and second, we compare the performance of parsimony and model-based approaches with morphological datasets. Our results imply that the grouping of Gnetales and angiosperms is largely the result of long branch attraction, consistent across a range of methodological approaches. Thus, there is a signal for the grouping of Gnetales with conifers in morphological matrices, but it was swamped by convergence between angiosperms and Gnetales, both situated on long branches. However, this effect becomes weaker in more recent analyses, as a result of addition and critical reassessment of characters. Even when a clade including angiosperms and Gnetales is still weakly supported by parsimony, model-based approaches favor a clade of Gnetales and conifers, presumably because they are more resistant to long branch attraction. Inclusion of fossil taxa weakens rather than strengthens support for a relationship of angiosperms and Gnetales. Our analyses finally reconcile morphology with molecules in favoring a relationship of Gnetales to conifers, and show that morphology may therefore be useful in reconstructing other aspects of the phylogenetic history of the seed plants

Research paper thumbnail of Editorial: Symbiotic Relationships as Shapers of Biodiversity

Frontiers in Ecology and Evolution, 2022

Research paper thumbnail of The Andes through time: evolution and distribution of Andean floras

Trends in Plant Science, 2022

The Andes are the world's most biodiverse mountain chain, encompassing a complex array of eco... more The Andes are the world's most biodiverse mountain chain, encompassing a complex array of ecosystems from tropical rainforests to alpine habitats. We provide a synthesis of Andean vascular plant diversity by estimating a list of all species with publicly available records, which we integrate with a phylogenetic dataset of 14 501 Neotropical plant species in 194 clades. We find that (i) the Andean flora comprises at least 28 691 georeferenced species documented to date, (ii) Northern Andean mid-elevation cloud forests are the most species-rich Andean ecosystems, (iii) the Andes are a key source and sink of Neotropical plant diversity, and (iv) the Andes, Amazonia, and other Neotropical biomes have had a considerable amount of biotic interchange through time.

Research paper thumbnail of Three‐dimensional X‐ray‐computed tomography of 3300‐ to 6000‐year‐old Citrullus seeds from Libya and Egypt compared to extant seeds throws doubts on species assignments

PLANTS, PEOPLE, PLANET, 2021

Societal Impact StatementThe watermelon (Citrullus lanatus subsp. vulgaris) is among the world&#3... more Societal Impact StatementThe watermelon (Citrullus lanatus subsp. vulgaris) is among the world's most important fruit crops. We here use C‐14 dating and morphometric analysis to test whether ancient seeds can be identified to species level, which would help document food expansion, innovation, and diversity in Northeastern Africa. We dated a Libyan seed to 6182–6001 calibrated years BP, making it the oldest Citrullus seed known. Morphometric analysis could not reliably assign ancient seeds to particular species, but several seeds showed breakage patterns characteristic of modern watermelon seeds cracked by human teeth. Our study contributes to the understanding of the early history of watermelon use by humans, who may have mostly snacked on the seeds, and cautions against the use of morphology alone to identify Citrullus archaeological samples.

Research paper thumbnail of Compartmentalization drives the evolution of symbiotic cooperation

Philosophical Transactions of the Royal Society B: Biological Sciences, 2020

Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with s... more Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid andVibrio, insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, ...

Research paper thumbnail of A chromosome-level genome of a Kordofan melon illuminates the origin of domesticated watermelons

Proceedings of the National Academy of Sciences, 2021

SignificanceWild progenitors of crops are important resources for breeding and for understanding ... more SignificanceWild progenitors of crops are important resources for breeding and for understanding domestication, but identifying them is difficult. Using an integrative approach, we discovered that a Sudanese form of melon with nonbitter whitish pulp, known as the Kordofan melon, is the closest relative of domesticated watermelons and a possible progenitor. To gain insights into the genetic changes that occurred from the progenitor to the domesticated watermelon, we assembled and annotated the genome of a Kordofan melon at the chromosome level. Our analyses imply that early farmers brought into cultivation already nonbitter watermelons, different from other domesticated Cucurbitaceae crops such as cucumber. The Kordofan melon genome is a significant new resource for watermelon breeding.

Research paper thumbnail of Hundreds of nuclear and plastid loci yield insights into orchid relationships

ABSTRACTPremise of the studyEvolutionary relationships in the species-rich Orchidaceae have histo... more ABSTRACTPremise of the studyEvolutionary relationships in the species-rich Orchidaceae have historically relied on organellar DNA sequences and limited taxon sampling. Previous studies provided a robust plastid-maternal phylogenetic framework, from which multiple hypotheses on the drivers of orchid diversification have been derived. However, the extent to which the maternal evolutionary history of orchids is congruent with that of the nuclear genome has remained uninvestigated.MethodsWe inferred phylogenetic relationships from 294 low-copy nuclear genes sequenced/obtained using the Angiosperms353 universal probe set from 75 species representing 69 genera, 16 tribes and 24 subtribes. To test for topological incongruence between nuclear and plastid genomes, we constructed a tree from 78 plastid genes, representing 117 genera, 18 tribes and 28 subtribes and compared them using a co-phylogenetic approach. The phylogenetic informativeness and support of the Angiosperms353 loci were compa...

Research paper thumbnail of Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants

The exuberant proliferation of herbivorous insects is attributed to their associations with plant... more The exuberant proliferation of herbivorous insects is attributed to their associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a unique opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide a...

Research paper thumbnail of Tradeoffs in the evolution of plant farming by ants

Proceedings of the National Academy of Sciences, 2020

Significance In human cultivation systems, farmers increasingly use technology to gather data for... more Significance In human cultivation systems, farmers increasingly use technology to gather data for evaluating tradeoffs between diverse—and sometimes conflicting—crop requirements to maximize yield. Some social insects have also evolved agricultural practices, but it is unknown how they evaluate local conditions to balance conflicting crop requirements. In the obligate farming symbiosis between ants and plants in Fijian rainforests, we show how ant farmers also face key tradeoffs in crop cultivation. While ants cannot simultaneously maximize all services to their crops, our work demonstrates that they cultivate crops in high-light conditions to maximize floral food rewards, despite the nitrogen costs of this strategy. Evaluation of crop tradeoffs plays a key role in the evolution of farming strategies.

Research paper thumbnail of Squamellaria: Plants domesticated by ants

PLANTS, PEOPLE, PLANET, 2019

Research paper thumbnail of World list ant plants 22 06 19 UPDATED

https://guillaumechomicki.wixsite.com/mysite/lab-resources, 2019

The world list of plant with ant domatia -- UPDATED

Research paper thumbnail of Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

eLife, Oct 27, 2022

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense deb... more The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined towards the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with past climate changes. Editor's evaluation This important work by Meseguer et al. depicts findings that substantially advance our understanding of clade diversification across major Neotropical bioregions. The evidence that summarises the evolutionary diversity dynamics of 150 time-calibrated clades of neotropical plants and animals data is convincingly presented with current state-of-the-art analyses. The work will be of interest to evolutionary biologists and biogeographers working to understand the origins of the most biodiverse land mass on the planet.

Research paper thumbnail of Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Zenodo (CERN European Organization for Nuclear Research), Jul 11, 2021

The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto r... more The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto relied heavily on plastid DNA sequences and limited taxon sampling. Previous studies have provided a robust plastid phylogenetic framework, which was used to classify orchids and investigate the drivers of orchid diversification. However, the extent to which phylogenetic inference based on the plastid genome is congruent with the nuclear genome has been only poorly assessed. METHODS: We inferred higher-level phylogenetic relationships of orchids based on likelihood and ASTRAL analyses of 294 low-copy nuclear genes sequenced using the Angiosperms353 universal probe set for 75 species (representing 69 genera, 16 tribes, 24 subtribes) and a concatenated analysis of 78 plastid genes for 264 species (117 genera, 18 tribes, 28 subtribes). We compared phylogenetic informativeness and support for the nuclear and plastid phylogenetic hypotheses. RESULTS: Phylogenetic inference using nuclear data sets provides well-supported orchid relationships that are highly congruent between analyses. Comparisons of nuclear gene trees and a plastid supermatrix tree showed that the trees are mostly congruent, but revealed instances of strongly supported phylogenetic incongruence in both shallow and deep time. The phylogenetic informativeness of individual Angiosperms353 genes is in general better than that of most plastid genes. CONCLUSIONS: Our study provides the first robust nuclear phylogenomic framework for Orchidaceae and an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely thoroughly documented: nuclear and plastid phylogenetic trees can contain strongly supported discordances, and this incongruence must be reconciled prior to interpretation in evolutionary studies, such as taxonomy, biogeography, and character evolution.

Research paper thumbnail of Chromosome numbers, Sudanese wild forms, and classification of the watermelon genus <i>Citrullus</i> , with 50 names allocated to seven biological species

Taxon, Nov 30, 2017

Watermelons are among the most important vegetable crops worldwide, but targeted breeding is hind... more Watermelons are among the most important vegetable crops worldwide, but targeted breeding is hindered by problems with Citrullus taxonomy. Here we clarify nomenclature and species relationships in Citrullus, its chromosome numbers, and the likely geographic region of watermelon domestication. We correct an erroneous chromosome count in recent literature, provide a count for an understudied species, and data on chromosome numbers for the entire genus. We also use a nuclear/ plastid locus phylogeny to summarize data on Citrullus sexual systems, loss of tendrils, life history, and geographic ranges. Key insights from new sequences are that (i) material of C. vulgaris var. "colocynthoides", collected by Schweinfurth in Egypt in 1882 represents the colocynth, C. colocynthis, and (ii) the citron or bitter watermelon, C. amarus, is indeed a separate species, not a subspecies of the dessert watermelon. Schweinfurth's varietal name, a nomen nudum, has been widely used for seeds as old as 5400 BP, and it now needs to be investigated whether these seeds are colocynths, watermelon or a hybrid. To help improve Citrullus taxonomy and nomenclature, we allocate some 50 scientific names to seven biological species, tabulate chromosome counts, and provide notes on misidentified germplasms traceable by accession numbers. More wildcollected herbarium-verified material from northeast Africa is urgently needed, especially given the discovery of Russian breeders that populations of wild "cordophanus" from Sudan are closer to the cultivated watermelon than are any other wild populations so far known.

Research paper thumbnail of Evolutionary Relationships and Biogeography of the Ant-Epiphytic Genus Squamellaria (Rubiaceae: Psychotrieae) and Their Taxonomic Implications

PLOS ONE, Mar 30, 2016

Ecological research on ant/plant symbioses in Fiji, combined with molecular phylogenetics, has br... more Ecological research on ant/plant symbioses in Fiji, combined with molecular phylogenetics, has brought to light four new species of Squamellaria in the subtribe Hydnophytinae of the Rubiaceae tribe Psychotrieae and revealed that four other species, previously in Hydnophytum, need to be transferred to Squamellaria. The diagnoses of the new species are based on morphological and DNA traits, with further insights from microCT scanning of flowers and leaf δ 13 C ratios (associated with Crassulacean acid metabolism). Our field and phylogenetic work results in a new circumscription of the genus Squamellaria, which now contains 12 species (to which we also provide a taxonomic key), not 3 as in the last revision. A clock-dated phylogeny and a model-testing biogeographic framework were used to infer the broader geographic history of rubiaceous ant plants in the Pacific, specifically the successive expansion of Squamellaria to Vanuatu, the Solomon Islands, and Fiji. The colonization of Vanuatu may have occurred from Fiji, when these islands were still in the same insular arc, while the colonization of the Solomon islands may have occurred after the separation of this island from the Fiji/Vanuatu arc. Some of these ant-housing epiphytes must have dispersed with their specialized ants, for instance attached to floating timber. Others acquired new ant symbionts on different islands.

Research paper thumbnail of The Origins and Drivers of Neotropical Diversity

bioRxiv (Cold Spring Harbor Laboratory), Feb 25, 2021

The origin of the outstanding Neotropical biodiversity is still debated. A comprehensive understa... more The origin of the outstanding Neotropical biodiversity is still debated. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here we define and evaluate four evolutionary scenarios assuming different diversity trajectories and drivers of Neotropical diversification. Relying on 150 phylogenies (12,512 species) of seed plants and tetrapods, we found that diversity mostly expanded through time (70% of the clades), but scenarios of saturated (21%) and declining (9%) diversity also account for a substantial proportion of Neotropical diversity. These scenarios occur indistinctly across the major regions, habitats, and altitudes of the Neotropics, suggesting no geographic structure of Neotropical diversification. On the contrary, diversification dynamics differ across taxonomic groups: plant diversity mostly expanded through time (88%), while for a significant fraction of tetrapods (43%) diversity accumulated at a slower pace or declined toward the present. These opposite evolutionary patterns reflect different capacities for plants and tetrapods to cope with environmental change, especially in relation to climate cooling. Our results suggest that the assembly of Neotropical diversity is a long, clade-specific, and complex process resulting from a combination of gradual and pulse dynamics associated with environmental stability and instability over macroevolutionary scales. .

Research paper thumbnail of Author response: Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

Research paper thumbnail of Diversification dynamics in the Neotropics through time, clades, and biogeographic regions

eLife

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense deb... more The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In ...

Research paper thumbnail of Genome Sequencing of up to 6,000-Year-OldCitrullusSeeds Reveals Use of a Bitter-Fleshed Species Prior to Watermelon Domestication

Molecular Biology and Evolution

Iconographic evidence from Egypt suggests that watermelon pulp was consumed there as a dessert by... more Iconographic evidence from Egypt suggests that watermelon pulp was consumed there as a dessert by 4,360 BP. Earlier archaeobotanical evidence comes from seeds from Neolithic settlements in Libya, but whether these were watermelons with sweet pulp or other forms is unknown. We generated genome sequences from 6,000- and 3,300-year-old seeds from Libya and Sudan, and from worldwide herbarium collections made between 1824 and 2019, and analyzed these data together with resequenced genomes from important germplasm collections for a total of 131 accessions. Phylogenomic and population-genomic analyses reveal that (1) much of the nuclear genome of both ancient seeds is traceable to West African seed-use “egusi-type” watermelon (Citrullus mucosospermus) rather than domesticated pulp-use watermelon (Citrullus lanatus ssp. vulgaris); (2) the 6,000-year-old watermelon likely had bitter pulp and greenish-white flesh as today found in C. mucosospermus, given alleles in the bitterness regulators ...

Research paper thumbnail of A highly contiguous, scaffold-level nuclear genome assembly for the Fever tree (Cinchona pubescens Vahl) as a novel resource for research in the Rubiaceae

BackgroundThe Andean Fever tree (Cinchona L.; Rubiaceae) is the iconic source of bioactive quinin... more BackgroundThe Andean Fever tree (Cinchona L.; Rubiaceae) is the iconic source of bioactive quinine alkaloids, which have been vital to treating malaria for centuries. C. pubescens Vahl, in particular, has been an essential source of income for several countries within its native range in north-western South America. However, an absence of available genomic resources is essential for placing the Cinchona species within the tree of life and setting the foundation for exploring the evolution and biosynthesis of quinine alkaloids.FindingsWe address this gap by providing the first highly contiguous and annotated nuclear and organelle genome assemblies for C. pubescens. Using a combination of ∼120 Gb of long sequencing reads derived from the Oxford Nanopore PromethION platform and 142 Gb of short-read Illumina data. Our nuclear genome assembly comprises 603 scaffolds comprising a total length of 904 Mb, and the completeness represents ∼85% of the genome size (1.1 Gb/1C). This draft genome...

Research paper thumbnail of Data from: Experimental signal dissection and method sensitivity analyses reaffirm the potential of fossils and morphology in the resolution of the relationship of angiosperms and Gnetales

The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmat... more The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmatic problems in plant evolution, with morphological analyses (which have usually included fossils) and molecular analyses pointing to very distinct topologies. Almost all morphology-based phylogenies group angiosperms with Gnetales and certain extinct seed plant lineages, while most molecular phylogenies link Gnetales with conifers. In this study, we investigate the phylogenetic signal present in published seed plant morphological datasets. We use parsimony, Bayesian inference, and maximum likelihood approaches, combined with a number of experiments with the data, to address the morphological-molecular conflict. First, we ask whether the lack of association of Gnetales with conifers in morphological analyses is due to an absence of signal or to the presence of competing signals, and second, we compare the performance of parsimony and model-based approaches with morphological datasets. Our results imply that the grouping of Gnetales and angiosperms is largely the result of long branch attraction, consistent across a range of methodological approaches. Thus, there is a signal for the grouping of Gnetales with conifers in morphological matrices, but it was swamped by convergence between angiosperms and Gnetales, both situated on long branches. However, this effect becomes weaker in more recent analyses, as a result of addition and critical reassessment of characters. Even when a clade including angiosperms and Gnetales is still weakly supported by parsimony, model-based approaches favor a clade of Gnetales and conifers, presumably because they are more resistant to long branch attraction. Inclusion of fossil taxa weakens rather than strengthens support for a relationship of angiosperms and Gnetales. Our analyses finally reconcile morphology with molecules in favoring a relationship of Gnetales to conifers, and show that morphology may therefore be useful in reconstructing other aspects of the phylogenetic history of the seed plants

Research paper thumbnail of Editorial: Symbiotic Relationships as Shapers of Biodiversity

Frontiers in Ecology and Evolution, 2022

Research paper thumbnail of The Andes through time: evolution and distribution of Andean floras

Trends in Plant Science, 2022

The Andes are the world's most biodiverse mountain chain, encompassing a complex array of eco... more The Andes are the world's most biodiverse mountain chain, encompassing a complex array of ecosystems from tropical rainforests to alpine habitats. We provide a synthesis of Andean vascular plant diversity by estimating a list of all species with publicly available records, which we integrate with a phylogenetic dataset of 14 501 Neotropical plant species in 194 clades. We find that (i) the Andean flora comprises at least 28 691 georeferenced species documented to date, (ii) Northern Andean mid-elevation cloud forests are the most species-rich Andean ecosystems, (iii) the Andes are a key source and sink of Neotropical plant diversity, and (iv) the Andes, Amazonia, and other Neotropical biomes have had a considerable amount of biotic interchange through time.

Research paper thumbnail of Three‐dimensional X‐ray‐computed tomography of 3300‐ to 6000‐year‐old Citrullus seeds from Libya and Egypt compared to extant seeds throws doubts on species assignments

PLANTS, PEOPLE, PLANET, 2021

Societal Impact StatementThe watermelon (Citrullus lanatus subsp. vulgaris) is among the world&#3... more Societal Impact StatementThe watermelon (Citrullus lanatus subsp. vulgaris) is among the world's most important fruit crops. We here use C‐14 dating and morphometric analysis to test whether ancient seeds can be identified to species level, which would help document food expansion, innovation, and diversity in Northeastern Africa. We dated a Libyan seed to 6182–6001 calibrated years BP, making it the oldest Citrullus seed known. Morphometric analysis could not reliably assign ancient seeds to particular species, but several seeds showed breakage patterns characteristic of modern watermelon seeds cracked by human teeth. Our study contributes to the understanding of the early history of watermelon use by humans, who may have mostly snacked on the seeds, and cautions against the use of morphology alone to identify Citrullus archaeological samples.

Research paper thumbnail of Compartmentalization drives the evolution of symbiotic cooperation

Philosophical Transactions of the Royal Society B: Biological Sciences, 2020

Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with s... more Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid andVibrio, insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, ...

Research paper thumbnail of A chromosome-level genome of a Kordofan melon illuminates the origin of domesticated watermelons

Proceedings of the National Academy of Sciences, 2021

SignificanceWild progenitors of crops are important resources for breeding and for understanding ... more SignificanceWild progenitors of crops are important resources for breeding and for understanding domestication, but identifying them is difficult. Using an integrative approach, we discovered that a Sudanese form of melon with nonbitter whitish pulp, known as the Kordofan melon, is the closest relative of domesticated watermelons and a possible progenitor. To gain insights into the genetic changes that occurred from the progenitor to the domesticated watermelon, we assembled and annotated the genome of a Kordofan melon at the chromosome level. Our analyses imply that early farmers brought into cultivation already nonbitter watermelons, different from other domesticated Cucurbitaceae crops such as cucumber. The Kordofan melon genome is a significant new resource for watermelon breeding.

Research paper thumbnail of Hundreds of nuclear and plastid loci yield insights into orchid relationships

ABSTRACTPremise of the studyEvolutionary relationships in the species-rich Orchidaceae have histo... more ABSTRACTPremise of the studyEvolutionary relationships in the species-rich Orchidaceae have historically relied on organellar DNA sequences and limited taxon sampling. Previous studies provided a robust plastid-maternal phylogenetic framework, from which multiple hypotheses on the drivers of orchid diversification have been derived. However, the extent to which the maternal evolutionary history of orchids is congruent with that of the nuclear genome has remained uninvestigated.MethodsWe inferred phylogenetic relationships from 294 low-copy nuclear genes sequenced/obtained using the Angiosperms353 universal probe set from 75 species representing 69 genera, 16 tribes and 24 subtribes. To test for topological incongruence between nuclear and plastid genomes, we constructed a tree from 78 plastid genes, representing 117 genera, 18 tribes and 28 subtribes and compared them using a co-phylogenetic approach. The phylogenetic informativeness and support of the Angiosperms353 loci were compa...

Research paper thumbnail of Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants

The exuberant proliferation of herbivorous insects is attributed to their associations with plant... more The exuberant proliferation of herbivorous insects is attributed to their associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a unique opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide a...

Research paper thumbnail of Tradeoffs in the evolution of plant farming by ants

Proceedings of the National Academy of Sciences, 2020

Significance In human cultivation systems, farmers increasingly use technology to gather data for... more Significance In human cultivation systems, farmers increasingly use technology to gather data for evaluating tradeoffs between diverse—and sometimes conflicting—crop requirements to maximize yield. Some social insects have also evolved agricultural practices, but it is unknown how they evaluate local conditions to balance conflicting crop requirements. In the obligate farming symbiosis between ants and plants in Fijian rainforests, we show how ant farmers also face key tradeoffs in crop cultivation. While ants cannot simultaneously maximize all services to their crops, our work demonstrates that they cultivate crops in high-light conditions to maximize floral food rewards, despite the nitrogen costs of this strategy. Evaluation of crop tradeoffs plays a key role in the evolution of farming strategies.

Research paper thumbnail of Squamellaria: Plants domesticated by ants

PLANTS, PEOPLE, PLANET, 2019