Evolutionary genomics of oceanic island radiations

Cerca, José; Cotoras, Darko D.; Bieker, Vanessa C.; De‐Kayne, Rishi; Vargas, Pablo; Fernández‐Mazuecos, Mario; López-Delgado, Julia; White, Oliver W.; Stervander, Martin; Geneva, Anthony J.; Andino, Juan Ernesto Guevara; Meier, Joana I.; Roeble, Lizzie; Brée, Baptiste; Patiño, Jairo; Guayasamín, Juan M.; Torres, María de Lourdes; Valdebenito, Hugo; Castañeda, María del Rosario; Chaves, Jaime A.; Díaz, Patricia Jaramillo; Valente, Luís; Knope, Matthew L.; Price, Jonathan P.; Baldwin, Bruce G.; Emerson, Brent C.; Rivas‐Torres, Gonzalo; Gillespie, Rosemary G.; Martin, Michael D.

doi:10.1016/j.tree.2023.02.003

Cited by 15 publications

(24 citation statements)

References 91 publications

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“…No trees grouped the Large Brown species as a monophyletic lineage. Despite these results, we found low values of gene and site concordance factors, together with short branches in the phylogenetic reconstructions, which may indicate high rates of incomplete lineage sorting in the radiation, an expected scenario in insular lineages where radiations often arise rapidly (Cerca et al, 2023;Choi et al, 2021).…”

Section: The Contribution Of Standing Genetic Variation To Repeated E...contrasting

confidence: 79%

“…Adaptive radiation is an evolutionary process in which a single ancestral lineage diversifies into multiple phenotypically distinct species adapted to different ecological niches. This process offers an excellent opportunity to investigate the links between phenotypic diversification and environmental adaptation (Gillespie et al, 2020; Schluter, 2000), as well as the genomic basis mediating evolutionary and ecological change (Cerca et al, 2023; De‐Kayne et al, 2022; Marques et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Multiple paths toward repeated phenotypic evolution in the spiny‐leg adaptive radiation (Tetragnatha; Hawai'i)

et al. 2023

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The repeated evolution of phenotypes provides clear evidence for the role of natural selection in driving evolutionary change. However, the evolutionary origin of repeated phenotypes can be difficult to disentangle as it can arise from a combination of factors such as gene flow, shared ancestral polymorphisms or mutation. Here, we investigate the presence of these evolutionary processes in the Hawaiian spiny‐leg Tetragnatha adaptive radiation, which includes four microhabitat‐specialists or ecomorphs, with different body pigmentation and size (Green, Large Brown, Maroon, and Small Brown). We investigated the evolutionary history of this radiation using 76 newly generated low‐coverage, whole‐genome resequenced samples, along with phylogenetic and population genomic tools. Considering the Green ecomorph as the ancestral state, our results suggest that the Green ecomorph likely re‐evolved once, the Large Brown and Maroon ecomorphs evolved twice and the Small Brown evolved three times. We found that the evolution of the Maroon and Small Brown ecomorphs likely involved ancestral hybridization events, while the Green and Large Brown ecomorphs likely evolved through novel mutations, despite a high rate of incomplete lineage sorting in the dataset. Our findings demonstrate that the repeated evolution of ecomorphs in the Hawaiian spiny‐leg Tetragnatha is influenced by multiple evolutionary processes.

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Section: The Contribution Of Standing Genetic Variation To Repeated E...contrasting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Multiple paths toward repeated phenotypic evolution in the spiny‐leg adaptive radiation (Tetragnatha; Hawai'i)

et al. 2023

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“…Such a population has the potential to undergo adaptive evolution in a novel environment [64,66] and repeated niche expansion, potentially resulting in diversification [e.g. 3,16]. Our case was unique in that both the back-colonized population and the source of introgression were produced through transcontinental colonization (Fig.…”

Section: Demography Affecting Genetic Variation Under Reverse Coloniz...mentioning

confidence: 99%

“…Islands, comprising 3.5% of the terrestrial land, contribute nearly 20% of global species richness and contribute more than 60% of extinct terrestrial species (Whittaker et al, 2017). It has been assumed that the small and isolated landmass and the unique environment of the island cause small population size with low genetic variation (Cerca et al, 2023) and specialization of genomes (e.g. Burga et al, 2017), likely leading to high risks of extinction (Frankham, 2005) and the evolutionary 'dead-end' (Vamosi et al, 2014).…”

Section: Main Text Introductionmentioning

confidence: 99%

Phylogenomics reveals an island as a genetic reservoir of a continental population

Aoki,

Senzaki,

Ando

et al. 2023

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AimIslands can become sources of continental biodiversity through reverse colonization. This is contradicted by the classic view of islands as sinks, because microevolution predicts difficulties in continental colonization by small island populations that are genetically depauperate. We fill this gap by examining historical demography that contributed to genetic variation of a continental population after reverse colonization. We exploit a rail species that likely evolved through reverse colonization, challenging the expectation that rails are the representatives of “end-of-colonization” on islands.LocationContinental East Asia (Russian Far East), Japanese ArchipelagoTaxaSwinhoe’s Rail (Coturnicops exquisitus)MethodsTo confirm reverse colonization, therein a continental population is derived from an island lineage, we reconstruct a complex phylogenetic relationship considering gene flow and introgression. We apply multiple methods using both high-throughput sequencing and mitochondrial datasets. We reconstruct a comprehensive demographic history of the species based on historical trajectory inference by Stairway Plot 2, fastsimcoal2 demographic modeling, and species distribution modeling. We assess genetic variation of the continental population and the key demographic process underlying them.ResultsThe continental population is inferred as a derived group within an island lineage, supporting reverse colonization. Demographic reconstruction suggests a significant population size decline through reverse colonization, with intraspecific gene flow from the island population. Introgression from an American sister species into the continental population is supported, which may be responsible for the unexpectedly high genetic variation observed.Main conclusionsUsing phylogenomics, we reconstruct reverse colonization associated with a complex history of population size changes and gene flow. Introgression, particularly, plays a pivotal role in rapidly restoring advantageous genetic variation for persistence and expansion on the continent post-reverse colonization. In theory, introgression assists adaptive radiation and diversification. Thus, our findings facilitate an understanding of the processes that islands contribute to global biodiversity, thereby bridging a gap between micro- and macroevolution.

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“…Answering these questions is not straightforward, because the speciation process is complex and involves different and interplaying mechanisms, such as geographic isolation, genetic drift, natural selection, and sexual selection (Gavrilets, 2004; Coyne, 2004; Gavrilets & Losos, 2009; Schluter, 2009; Nosil et al, 2009). Since access to genomic data is increasing rapidly, the investigation of mechanisms underlying diversification and speciation has been extended to numerous taxa, environments, and evolutionary stages (Seehausen et al, 2014; Berner & Salzburger, 2015; Cerca et al, 2023). Studies have identified loci promoting ecological divergence and, eventually, speciation (e.g., Malinsky et al, 2015; Payseur & Rieseberg, 2016).…”

Section: Introductionmentioning

confidence: 99%

Recurrent gene flow events shaped the diversification of the clownfish skunk complex

Marcionetti,

Bertrand,

Cortesi

et al. 2023

Preprint

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Clownfish (subfamily Amphiprioninae) are an iconic group of coral reef fish that evolved a mutualistic interaction with sea anemones, which was shown to have triggered the adaptive radiation of the group. Within clownfishes, the skunk complex is particularly interesting as, besides ecological speciation, gene flow between species and hybrid speciation are suggested to have shaped the diversification of the group. We investigated, for the first time, the mechanisms underlying the diversification of this complex. By taking advantage of their disjunct geographical distribution, we obtained whole-genome data of sympatric and allopatric populations of the three main species of the complex (Amphiprion akallopisos, A. perideraion and A. sandaracinos). We examined the population structure, genomic divergence patterns and introgression signals, and performed demographic modeling to identify the most realistic diversification scenario. We excluded scenarios of strict isolation, of hybrid origin of A. sandaracinos, and ruled out the presence of extensive gene flow in sympatry. We discovered moderate gene flow from A. perideraion to the ancestor of A. akallopisos + A. sandaracinos and weak gene flow between the species in the Indo-Australian Archipelago throughout the diversification process of the group. We identified introgressed regions in A. sandaracinos and detected two large regions of high divergence in A. perideraion, likely maintained by the disruption of recombination. Altogether, our results show that ancestral hybridization events shaped the group's diversification. However, more recent gene flow is less pervasive than initially thought and suggests a role of host repartition or behavioral barriers in maintaining the genetic identity of the species in sympatry.

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Evolutionary genomics of oceanic island radiations

Cited by 15 publications

References 91 publications

Multiple paths toward repeated phenotypic evolution in the spiny‐leg adaptive radiation (Tetragnatha; Hawai'i)

Multiple paths toward repeated phenotypic evolution in the spiny‐leg adaptive radiation (Tetragnatha; Hawai'i)

Phylogenomics reveals an island as a genetic reservoir of a continental population

Recurrent gene flow events shaped the diversification of the clownfish skunk complex

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