The Taxon Cycle: how current invasive species may become endemics on islands

The taxon cycle seeks to explain how the biodiversity on islands arises. The theory proposes that patterns of biodiversity across oceanic archipelagos can be explained by new taxa consistently arriving on islands in more disturbed coastal habitats and displacing earlier colonists to inland habitats. Over time, these early colonizers become endemic to single islands with increasingly narrow distributions due to habitat specialization. When these narrow range endemics eventually go extinct, several waves of new colonizers have arrived and displaced their predecessors, ensuring the cycle continues.

The theory was first proposed by the late Edward O Wilson based on his work on ants in Melanesia. He proposed 4 major stages in this cycle (Fig. 1). First, a taxon evolves a characteristic that allows it to disperse effectively across oceans and colonizes coastal habitats of archipelagos across a wide geographic range. During the second stage, the taxon adapts to habitats further inland on islands and populations on different archipelagos and/or islands begin to differentiate. At the third stage, this differentiation has resulted in the formation of different species, with reduced dispersal abilities contributing to this. However, speciation is also linked to greater geographic isolation caused by displacement from coastal habitats by new colonizers and increasing habitat specialization. Finally, the distribution of the taxon continues to contract until they are endemic restricted to higher elevations and/or become extinct.

Fig. 1: Illustration of the four stage of the taxon cycle using cycads (Cycas, Cycadaceae) in the Pacific). Stage 2 corresponds to the current distribution of the genus and includes a picture of a coastal population of Cycas seemannii – all other stages are hypothetical. Stage 1: the Pacific Cycas lineage has recently colonized the region and has little morphological and genetic differentiation across its distribution. Stage 2: groups within the lineage begin to differentiate among archipelagos. Stage 3: Speciation and range contractions, as well as extinctions on several island have produced several, more isolated species. The species have undergone an ecological shift from coastal to inland habitats. Stage 4: Further range contractions and extinctions have produced a highly fragmented distribution with species restricted to a few islands and specialized habitats. (Adapted from: Keppel & Ibanez (in press) Biogeography: Island biotas changing through space and time, IN: The Pacific Islands: Environment and Society (3rd Edition), University of Hawaii Press)

Molecular studies have provided good support for the taxon cycle over the last decades and there are examples that support for theoccurrence of the various stages. Work by Matos-Maravi and colleagues on trap-jaw ants provided evidence for the first stage: habitat shifts from inland habitats to more open habitats tended to increase dispersal abilities. Oliver and colleagues found support for inland habitats being more likely to support older lineages of the geckos studied, as would be expected based on stages 2 and 3. Looking at cuckooshrike birds and their relatives, Pepke and colleagues found support for the fourth stage, showing that there are fewer older species that inhabit larger islands at higher elevations compared to younger ones.

Our recent meta-analysis combined molecular studies throughout the Pacific to more broadly investigate the predictions of the taxon cycle and found strong support. Overall, the majority of taxa investigated arrived relatively recently (within the last 5 million years), supporting the consistent flow of new colonizers to displace earlier colonizers (Fig. 2). Interestingly, we found that this trend was less pronounced on the oldest archipelagos studies: Fiji and New Caledonia. This suggests that as islands age their habitats fill up, reducing the chances of successfully displacing an earlier colonizer inland. Hence the taxon cycle may slow on old archipelagos.

Fig 2: Plots indicating the estimated colonizations times for multiple lineages for 16 Pacific archipealgos, with the thickness of the coloured shapes indicating the proportion of lineages corresponding to a particular age. Asterisks indicate the estimated age of archipelagos. Archipelagos: Aut, Austral Islands; Bis, Bismarck Archipelago; Car, Caroline Islands; Coo, Cook Islands; Fij, Fiji; Gal, Galapagos Islands; Haw, Hawaii; LHo, Lord Howe Islands; Mai, Mariana Islands; Maq, Marquesas; N, number of aged colonization events included; NCa, New Caledonia; Sam, Samoa; Soc, Society Islands; Sol, Solomon Islands; Ton, Tonga; Van, Vanuatu. Source: Keppel & Ibanez (2024) J. System. Evol. 62:201-214.

There are also implications of the taxon cycle to species currently considered invasive on islands. While in the past new species arrived via natural processes, such as birds transporting seeds between islands, most current colonization events are faciliated by humans. As a result, islands have been rapidly accummulating non-native species. While many of these species introduced by humans remain currently restricted to disturbed, non-native habitats, the taxon cycle theory suggests that some of these introduced species will, over time, adapt to native habitats. For example, the widely planted (as an ornamental) African Tulip tree, Spathodea campanulata (Bignoniaceae), has been colonizing habitats dominated by native species in the Bismarck Archipelago (Papua New Guinea), Fiji, French Polynesia, and other Pacific archipelagos. The results of our meta-analysis suggest that the chance of invasive species establishing in native habitats should be lower on older islands with less vacant niche space.

The taxon cycle theory further predicts that some of the non-native species will eventually evolve into species endemic to different archipelagos. This of course will raise challenging questions for the management of invasive species and the conservation of native species. Should we still aim to eradicate a population that originated from a human introduction but is now morphologically and genetically unique from its source population? If not, should it be considered as high a priority for conservation as other endemic taxa that arrived much earlier via natural processes?

Further reading about the taxon cycle:

Keppel G, Nge FJ, & Ibanez T (2024) Slowing taxon cycle can explain biodiversity patterns on islands: Insights into the biogeography of the tropical South Pacific from molecular data. Journal of Systematics and Evolution 62: 201-214. https://doi.org/10.1111/jse.13026

Matos-Maraví P, et al. (2018) Taxon cycle predictions supported by model-based inference in Indo-Pacific trap-jaw ants (Hymenoptera: Formicidae: Odontomachus). Molecular Ecology 27: 4090-4107. https://doi.org/10.1111/mec.14835

Pepke ML, Irestedt M, Fjeldså J, Rahbek C, & Jønsson KA (2019) Reconciling supertramps, great speciators and relict species with the taxon cycle stages of a large island radiation (Aves: Campephagidae). Journal of Biogeography 46: 1214-1225. https://doi.org/10.1111/jbi.13577

Oliver PM, Brown RM, Kraus F, Rittmeyer E, Travers SL, & Siler CD (2018) Lizards of the lost arcs: mid-Cenozoic diversification, persistence and ecological marginalization in the West Pacific. Proceedings of the Royal Society B: Biological Sciences 285: 20171760. https://doi.org/10.1098/rspb.2017.1760

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