Sunday, October 17, 2021

When adaptive radiations collide: Different evolutionary trajectories between and within island and mainland lizard clades




View ORCID ProfileAustin H. Patton, Luke J. Harmon, María del Rosario Castañeda, Hannah K. Frank, View ORCID ProfileColin M. Donihue, View ORCID ProfileAnthony Herrel, and Jonathan B. Losos

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PNAS October 19, 2021 118 (42) e2024451118; https://doi.org/10.1073/pnas.2024451118

Contributed by Jonathan B. Losos, December 14, 2020 (sent for review December 14, 2020; reviewed by Michael E. Alfaro and Frank T. Burbrink)
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Significance

Isolated and infrequently colonized, islands harbor many of nature’s most renowned evolutionary radiations. Despite this evolutionary exuberance, island occupation has long been considered irreversible: The much tougher competitive and predatory milieu on mainlands prevents colonization, much less evolutionary diversification, from islands to continents. To test these postulates, we examined neotropical Anolis lizards, asking what happens when mainland and island evolutionary radiations collide. Far from being a dead end, we show that island-to-mainland colonization seeded an extensive radiation that achieved its ecomorphological disparity in ways distinct from their island ancestors. Moreover, when the incumbent and island-derived radiations collided, the ensuing interactions favored the latter, together highlighting a persistent role of both historical contingency and determinism in adaptive radiation.

Abstract

Oceanic islands are known as test tubes of evolution. Isolated and colonized by relatively few species, islands are home to many of nature’s most renowned radiations from the finches of the Galápagos to the silverswords of the Hawaiian Islands. Despite the evolutionary exuberance of insular life, island occupation has long been thought to be irreversible. In particular, the presumed much tougher competitive and predatory milieu in continental settings prevents colonization, much less evolutionary diversification, from islands back to mainlands. 

To test these predictions, we examined the ecological and morphological diversity of neotropical Anolis lizards, which originated in South America, colonized and radiated on various islands in the Caribbean, and then returned and diversified on the mainland.

We focus in particular on what happens when mainland and island evolutionary radiations collide. We show that extensive continental radiations can result from island ancestors and that the incumbent and invading mainland clades achieve their ecological and morphological disparity in very different ways. Moreover, we show that when a mainland radiation derived from island ancestors comes into contact with an incumbent mainland radiation the ensuing interactions favor the island-derived clade.

Anolis
macroevolution
adaptive radiation
convergence
diversification

Footnotes


1A.H. and J.B.L. contributed equally to this work.
2To whom correspondence may be addressed. Email: anthony.herrel@mnhn.fr or losos@wustl.edu.
Accepted August 12, 2021.


This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2018.


Author contributions: A.H.P., L.J.H., and J.B.L. designed research; A.H.P., M.d.R.C., H.K.F., C.M.D., A.H., and J.B.L. performed research; A.H.P. analyzed data; and A.H.P., L.J.H., A.H., and J.B.L. wrote the paper.


Reviewers: M.E.A., University of California, Los Angeles; and F.T.B., American Museum of Natural History.


The authors declare no competing interest.


See QnAs, e2116186118, in vol. 118, issue 42.


This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2024451118/-/DCSupplemental.

Data Availability

Scripts and ecological and morphological measurements have been deposited in GitHub (https://github.com/austinhpatton/AnolisRadiation) (80). Ecological, morphological, and all other study data are included in the article and/or supporting information.

REFERENCES ARE IN THE ARTICLE LINKED ABOVE

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