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Fulltext Out of Borneo: biogeography, phylogeny and divergence date estimates of Artocarpus (Moraceae)

Williams EW, Gardner EM, Harris R, Chaveerach A, Pereira JT, Zerega NJ

Ann Bot, 2017 03 01;119(4):611-627.
PMID: 28073771 DOI: 10.1093/aob/mcw249

Background and Aims: The breadfruit genus ( Artocarpus , Moraceae) includes valuable underutilized fruit tree crops with a centre of diversity in Southeast Asia. It belongs to the monophyletic tribe Artocarpeae, whose only other members include two small neotropical genera. This study aimed to reconstruct the phylogeny, estimate divergence dates and infer ancestral ranges of Artocarpeae, especially Artocarpus , to better understand spatial and temporal evolutionary relationships and dispersal patterns in a geologically complex region.
Methods: To investigate the phylogeny and biogeography of Artocarpeae, this study used Bayesian and maximum likelihood approaches to analyze DNA sequences from six plastid and two nuclear regions from 75% of Artocarpus species, both neotropical Artocarpeae genera, and members of all other Moraceae tribes. Six fossil-based calibrations within the Moraceae family were used to infer divergence times. Ancestral areas and estimated dispersal events were also inferred.
Key Results: Artocarpeae, Artocarpus and four monophyletic Artocarpus subgenera were well supported. A late Cretaceous origin of the Artocarpeae tribe in the Americas is inferred, followed by Eocene radiation of Artocarpus in Asia, with the greatest diversification occurring during the Miocene. Borneo is reconstructed as the ancestral range of Artocarpus , with dozens of independent in situ diversification events inferred there, as well as dispersal events to other regions of Southeast Asia. Dispersal pathways of Artocarpus and its ancestors are proposed.
Conclusions: Borneo was central in the diversification of the genus Artocarpus and probably served as the centre from which species dispersed and diversified in several directions. The greatest amount of diversification is inferred to have occurred during the Miocene, when sea levels fluctuated and land connections frequently existed between Borneo, mainland Asia, Sumatra and Java. Many species found in these areas have extant overlapping ranges, suggesting that sympatric speciation may have occurred. By contrast, Artocarpus diversity east of Borneo (where many of the islands have no historical connections to the landmasses of the Sunda and Sahul shelves) is unique and probably the product of over water long-distance dispersal events and subsequent diversification in allopatry. This work represents the most comprehensive Artocarpus phylogeny and biogeography study to date and supports Borneo as an evolutionary biodiversity hotspot.
Fulltext Origin and diversity of an underutilized fruit tree crop, cempedak (Artocarpus integer, Moraceae)

Wang MMH, Gardner EM, Chung RCK, Chew MY, Milan AR, Pereira JT, et al.

Am J Bot, 2018 05;105(5):898-914.
PMID: 29874392 DOI: 10.1002/ajb2.1094

PREMISE OF THE STUDY: Underutilized crops and their wild relatives are important resources for crop improvement and food security. Cempedak [Artocarpus integer (Thunb). Merr.] is a significant crop in Malaysia but underutilized elsewhere. Here we performed molecular characterization of cempedak and its putative wild relative bangkong (Artocarpus integer (Thunb). Merr. var. silvestris Corner) to address questions regarding the origin and diversity of cempedak.
METHODS: Using data from 12 microsatellite loci, we assessed the genetic diversity and genetic/geographic structure for 353 cempedak and 175 bangkong accessions from Malaysia and neighboring countries and employed clonal analysis to characterize cempedak cultivars. We conducted haplotype network analyses on the trnH-psbA region in a subset of these samples. We also analyzed key vegetative characters that reportedly differentiate cempedak and bangkong.
KEY RESULTS: We show that cempedak and bangkong are sister taxa and distinct genetically and morphologically, but the directionality of domestication origin is unclear. Genetic diversity was generally higher in bangkong than in cempedak. We found a distinct genetic cluster for cempedak from Borneo as compared to cempedak from Peninsular Malaysia. Finally, cempedak cultivars with the same names did not always share the same genetic fingerprint.
CONCLUSIONS: Cempedak origins are complex, with likely admixture and hybridization with bangkong, warranting further investigation. We provide a baseline of genetic diversity of cempedak and bangkong in Malaysia and found that germplasm collections in Malaysia represent diverse coverage of the four cempedak genetic clusters detected.
Fulltext Paralogs and off-target sequences improve phylogenetic resolution in a densely-sampled study of the breadfruit genus (Artocarpus, Moraceae)

Gardner EM, Johnson MG, Pereira JT, Puad ASA, Arifiani D, Wickett NJ, et al.

Syst Biol, 2020 Sep 24;70(3):558-75.
PMID: 32970819 DOI: 10.1093/sysbio/syaa073

We present a 517-gene phylogenetic framework for the breadfruit genus Artocarpus (ca. 70 spp., Moraceae), making use of silica-dried leaves from recent fieldwork and herbarium specimens (some up to 106 years old) to achieve 96% taxon sampling. We explore issues relating to assembly, paralogous loci, partitions, and analysis method to reconstruct a phylogeny that is robust to variation in data and available tools. While codon partitioning did not result in any substantial topological differences, the inclusion of flanking non-coding sequence in analyses significantly increased the resolution of gene trees. We also found that increasing the size of datasets increased convergence between analysis methods but did not reduce gene tree conflict. We optimized the HybPiper targeted-enrichment sequence assembly pipeline for short sequences derived from degraded DNA extracted from museum specimens. While the subgenera of Artocarpus were monophyletic, revision is required at finer scales, particularly with respect to widespread species. We expect our results to provide a basis for further studies in Artocarpus and provide guidelines for future analyses of datasets based on target enrichment data, particularly those using sequences from both fresh and museum material, counseling careful attention to the potential of off-target sequences to improve resolution.
Fulltext Museomics for reconstructing historical floristic exchanges: Divergence of stone oaks across Wallacea

Strijk JS, Binh HT, Ngoc NV, Pereira JT, Slik JWF, Sukri RS, et al.

PLoS One, 2020;15(5):e0232936.
PMID: 32442164 DOI: 10.1371/journal.pone.0232936

Natural history collections and tropical tree diversity are both treasure troves of biological and evolutionary information, but their accessibility for scientific study is impeded by a number of properties. DNA in historical specimens is generally highly fragmented, complicating the recovery of high-grade genetic material. Furthermore, our understanding of hyperdiverse, wide-spread tree assemblages is obstructed by extensive species ranges, fragmented knowledge of tropical tree diversity and phenology, and a widespread lack of species-level diagnostic characters, prohibiting the collecting of readily identifiable specimens which can be used to build, revise or strengthen taxonomic frameworks. This, in turn, delays the application of downstream conservation action. A sizable component of botanical collections are sterile-thus eluding identification and are slowing down progress in systematic treatments of tropical biodiversity. With rapid advances in genomics and bioinformatic approaches to biodiversity research, museomics is emerging as a new field breathing life into natural collections that have been built up over centuries. Using MIGseq (multiplexed ISSR genotyping by sequencing), we generated 10,000s of short loci, for both freshly collected materials and museum specimens (aged >100 years) of Lithocarpus-a widespread tropical tree genus endemic to the Asian tropics. Loci recovery from historical and recently collected samples was not affected by sample age and preservation history of the study material, underscoring the reliability and flexibility of the MIGseq approach. Phylogenomic inference and biogeographic reconstruction across insular Asia, highlights repeated migration and diversification patterns between continental regions and islands. Results indicate that co-occurring insular species at the extremity of the distribution range are not monophyletic, raising the possibility of multiple independent dispersals along the outer edge of Wallacea. This suggests that dispersal of large seeded tree genera throughout Malesia and across Wallacea may have been less affected by large geographic distances and the presence of marine barriers than generally assumed. We demonstrate the utility of MIGseq in museomic studies using non-model taxa, presenting the first range-wide genomic assessment of Lithocarpus and tropical Fagaceae as a proof-of-concept. Our study shows the potential for developing innovative genomic approaches to improve the capture of novel evolutionary signals using valuable natural history collections of hyperdiverse taxa.
Incorporating connectivity into conservation planning for the optimal representation of multiple species and ecosystem services

Williams SH, Scriven SA, Burslem DFRP, Hill JK, Reynolds G, Agama AL, et al.

Conserv Biol, 2020 08;34(4):934-942.
PMID: 31840279 DOI: 10.1111/cobi.13450

Conservation planning tends to focus on protecting species' ranges or landscape connectivity but seldom both-particularly in the case of diverse taxonomic assemblages and multiple planning goals. Therefore, information on potential trade-offs between maintaining landscape connectivity and achieving other conservation objectives is lacking. We developed an optimization approach to prioritize the maximal protection of species' ranges, ecosystem types, and forest carbon stocks, while also including habitat connectivity for range-shifting species and dispersal corridors to link protected area. We applied our approach to Sabah, Malaysia, where the state government mandated an increase in protected-area coverage of approximately 305,000 ha but did not specify where new protected areas should be. Compared with a conservation planning approach that did not incorporate the 2 connectivity features, our approach increased the protection of dispersal corridors and elevational connectivity by 13% and 21%, respectively. Coverage of vertebrate and plant species' ranges and forest types were the same whether connectivity was included or excluded. Our approach protected 2% less forest carbon and 3% less butterfly range than when connectivity features were not included. Hence, the inclusion of connectivity into conservation planning can generate large increases in the protection of landscape connectivity with minimal loss of representation of other conservation targets.
Fulltext Echoes of ancient introgression punctuate stable genomic lineages in the evolution of figs

Gardner EM, Bruun-Lund S, Niissalo M, Chantarasuwan B, Clement WL, Geri C, et al.

Proc Natl Acad Sci U S A, 2023 Jul 11;120(28):e2222035120.
PMID: 37399402 DOI: 10.1073/pnas.2222035120

Studies investigating the evolution of flowering plants have long focused on isolating mechanisms such as pollinator specificity. Some recent studies have proposed a role for introgressive hybridization between species, recognizing that isolating processes such as pollinator specialization may not be complete barriers to hybridization. Occasional hybridization may therefore lead to distinct yet reproductively connected lineages. We investigate the balance between introgression and reproductive isolation in a diverse clade using a densely sampled phylogenomic study of fig trees (Ficus, Moraceae). Codiversification with specialized pollinating wasps (Agaonidae) is recognized as a major engine of fig diversity, leading to about 850 species. Nevertheless, some studies have focused on the importance of hybridization in Ficus, highlighting the consequences of pollinator sharing. Here, we employ dense taxon sampling (520 species) throughout Moraceae and 1,751 loci to investigate phylogenetic relationships and the prevalence of introgression among species throughout the history of Ficus. We present a well-resolved phylogenomic backbone for Ficus, providing a solid foundation for an updated classification. Our results paint a picture of phylogenetically stable evolution within lineages punctuated by occasional local introgression events likely mediated by local pollinator sharing, illustrated by clear cases of cytoplasmic introgression that have been nearly drowned out of the nuclear genome through subsequent lineage fidelity. The phylogenetic history of figs thus highlights that while hybridization is an important process in plant evolution, the mere ability of species to hybridize locally does not necessarily translate into ongoing introgression between distant lineages, particularly in the presence of obligate plant-pollinator relationships.
Evolution of endemism on a young tropical mountain

Merckx VS, Hendriks KP, Beentjes KK, Mennes CB, Becking LE, Peijnenburg KT, et al.

Nature, 2015 Aug 20;524(7565):347-50.
PMID: 26266979 DOI: 10.1038/nature14949

Tropical mountains are hot spots of biodiversity and endemism, but the evolutionary origins of their unique biotas are poorly understood. In varying degrees, local and regional extinction, long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities. Also, it is debated whether mountain endemics mostly originate from local lowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere. Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu in Sabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), and comprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shifts from lower to higher vegetation zones in this latter group were rare. These insights could improve forecasts of the likelihood of extinction and 'evolutionary rescue' in montane biodiversity hot spots under climate change scenarios.