New Caledonian lineages of Psychotria (Rubiaceae) reveal different evolutionary histories and the largest documented plant radiation for the archipelago

Barrabé, Laure; Maggia, Laurent; Pillon, Yohan; Rigault, Frédéric; Mouly, Arnaud; Davis, Aaron P.; Buerki, Sven

doi:10.1016/j.ympev.2013.10.020

Cited by 54 publications

(69 citation statements)

References 115 publications

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“…Our genomic study is fully consistent with other studies that have dated the origin of the leaf nodule symbiosis back to the Miocene (in a range of 5.5-13.82 Mya) (Supplementary Figure S5) (see Supplementary Information Methods) (Lemaire et al, 2011;Barrabé et al, 2014). The obligate interaction between leaf nodule symbionts and their host plant could have evolved from an initial facultative and commensal association ( Figure 5).…”

Section: Discussionsupporting

confidence: 89%

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

Pinto‐Carbó¹,

Sieber²,

Dessein³

et al. 2016

The ISME Journal

105

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Bacteria of the genus Burkholderia establish an obligate symbiosis with plant species of the Rubiaceae and Primulaceae families. The bacteria, housed within the leaves, are transmitted hereditarily and have not yet been cultured. We have sequenced and compared the genomes of eight bacterial leaf nodule symbionts of the Rubiaceae plant family. All of the genomes exhibit features consistent with genome erosion. Genes potentially involved in the biosynthesis of kirkamide, an insecticidal C7N aminocyclitol, are conserved in most Rubiaceae symbionts. However, some have partially lost the kirkamide pathway due to genome erosion and are unable to synthesize the compound. Kirkamide synthesis is therefore not responsible for the obligate nature of the symbiosis. More importantly, we find evidence of intra-clade horizontal gene transfer (HGT) events affecting genes of the secondary metabolism. This indicates that substantial gene flow can occur at the early stages following host restriction in leaf nodule symbioses. We propose that host-switching events and plasmid conjugative transfers could have promoted these HGTs. This genomic analysis of leaf nodule symbionts gives, for the first time, new insights in the genome evolution of obligate symbionts in their early stages of the association with plants.

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Section: Discussionsupporting

confidence: 89%

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

Pinto‐Carbó¹,

Sieber²,

Dessein³

et al. 2016

The ISME Journal

105

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“…The pattern observed here is similar to the multiple colonizations of Psychotria s.l. (Psychotrieae‐Palicoureae) in New Caledonia where four colonizers gave rise to one, four, four and 78 species (Barrabé et al., ).…”

Section: Discussionmentioning

confidence: 99%

Multiple colonizations, hybridization and uneven diversification in Cyrtandra (Gesneriaceae) lineages on Hawai'i Island

Johnson

Pillon

Sakishima

et al. 2019

Journal of Biogeography

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Aim The diversity and composition of species pools within oceanic archipelagos is determined by a combination of colonization, abiotic tolerance, in situ diversification, biotic interactions and extinction. The signature of biogeographic events and evolutionary processes, however, may be masked by recent coalescence and hybridization between closely related species. We used the species‐rich plant genus Cyrtandra (Gesneriaceae) to investigate the roles of colonization and hybridization in shaping community assemblages on the geologically young Hawai'i Island. Location Hawaiian Islands. Taxon Cyrtandra (Gesneriaceae). Methods We sampled 29 Cyrtandra taxa and putative hybrids across the main Hawaiian Islands and generated single nucleotide polymorphisms (SNPs) from nine single‐copy nuclear genes. Maximum likelihood and Bayesian inference were used to reconstruct phylogenetic relationships, divergence times were estimated using secondary calibrations and island ages, and ancestral area estimation was done using likelihood models. Lastly, we used a Bayesian population assignment test and principal components analysis to infer population genetic structure. Results Cyrtandra colonization of the main Hawaiian Islands appears to have followed the progression rule, whereby the oldest high Hawaiian Islands (Kaua'i and O'ahu) were colonized first, followed by colonization of the younger islands as habitat became available. Hawai'i Island was colonized four times, with two dispersal events from O'ahu and two from Maui Nui. The different colonization events gave rise to significantly uneven numbers of species, and hybridization among the incipient lineages was detected in the form of intermediate genotypes. Main conclusions Our investigation into community assembly in a species‐rich plant genus on a geologically young oceanic island revealed a history of multiple colonizations and hybridization among colonizing lineages. The rapid diversification (3.5 species/My) of one of four Cyrtandra lineages on Hawai'i Island may be the result of hybridization between genetically diverse lineages that stem from independent colonization events. Multiple colonization events followed by a merging of lineages may be particularly common during early‐stage community assembly on islands and, through the generation of genetic variation, may be especially important for species diversification.

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“…A sampling of outgroups (in the tribe Psychotrieae) was selected on the basis of ref. 64. Voucher information is reported in SI Appendix, Table S2.…”

Section: Methodsmentioning

confidence: 99%

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Chomicki

Renner

2017

Proc. Natl. Acad. Sci. U.S.A.

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Mutualisms that involve symbioses among specialized partners may be more stable than mutualisms among generalists, and theoretical models predict that in many mutualisms, partners exert reciprocal stabilizing selection on traits directly involved in the interaction. A corollary is that mutualism breakdown should increase morphological rates of evolution. We here use the largest ant-plant clade (Hydnophytinae), with different levels of specialization for mutualistic ant symbionts, to study the ecological context of mutualism breakdown and the response of a key symbiosis-related trait, domatium entrance hole size, which filters symbionts by size. Our analyses support three predictions from mutualism theory. First, all 12 losses apparently only occur from a generalist symbiotic state. Second, mutualism losses occurred where symbionts are scarce, in our system at high altitudes. Third, domatium entrance hole size barely changes in specialized symbiotic species, but evolves rapidly once symbiosis with ants has broken down, with a "morphorate map" revealing that hotspots of entrance hole evolution are clustered in high-altitude areas. Our study reveals that mutualistic strategy profoundly affects the pace of morphological change in traits involved in the interaction and suggests that shifts in partners' relative abundances may frequently drive reversions of generalist mutualisms to autonomy. mutualism | symbiosis | morphology | comparative phylogenetic methods | ants U nderstanding how mutualisms arise, persist, or break down is a major focus in ecology and evolutionary biology (1-3). Symbiotic mutualisms can revert to the free-living state if the costto-benefit ratio shifts so that costs outweigh benefits. There are three main pathways through which mutualism can break down, namely, extinction of the partner, reversion to the free-living state, or shift to parasitism (2). Extinction of one partner in an obligate mutualism should entail the extinction of the other, whereas in a facultative mutualism, extinction might lead to a reversion to autonomy (4-8), but these predictions have limited support from empirical studies. Similarly, mutualism could also break down if one partner becomes scarce, which may be especially important in laterally transferred symbioses where partners disperse independently and the interaction needs to be reestablished at each generation, involving vulnerable stages for both. Mutualisms can also break down by shifting to parasitism. Such shifts are predicted by theory (9, 10) because reducing or stopping reciprocation increases the fitness of the cheating partner (11)(12)(13)(14). Phylogenetically unrelated freeloaders may also disrupt a mutualism by exploiting it (15-18). Finally, mutualism can break down if benefits can be obtained cheaply or freely from the environment, for example, when plants involved in mycorrhizal or rhizobia symbioses grow in nutrient-rich soils (19,20) or when antiherbivore defense by ant mutualists is no longer required (21). Most of these theoretical expectations ab...

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New Caledonian lineages of Psychotria (Rubiaceae) reveal different evolutionary histories and the largest documented plant radiation for the archipelago

Cited by 54 publications

References 115 publications

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

Multiple colonizations, hybridization and uneven diversification in Cyrtandra (Gesneriaceae) lineages on Hawai'i Island

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

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