Comparing Adaptive Radiations Across Space, Time, and Taxa

Abstract

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

Figure 1.

Model systems studied by contributors of the AGA 2018 President’s Symposium: Origins of Adaptive Radiation. Yellow dots represent areas where field studies have been conducted and do not accurately represent the full geographic distribution of each group. Anti-clockwise from top-right: Mediterranean labrine wrasses, Alpine charr (Salvelinus umbla complex), European Alpine whitefish (Coregonus spp.), Caribbean Anolis lizards, San Salvador pupfish (Cyprinodon sp.), spadefoot toads (Spea sp.), stickleback fish (Gasterosteus aculeatus), Hawaiian spiders, Laupala crickets, Nesophrosyne leafhoppers, Hawaiian Metrosideros plants, Hyposmocoma moths, Hawaiian honeycreepers, Hawaiian Bidens, Galapagos land snails (Bulimulus sp.), Darwin’s finches (Geospiza sp.), mainland Anolis lizards, Heliconius butterflies, Nesospiza finches of the Tristan da Cunha archipelago, African Great Lake cichlids, and Cameroon crater lake cichlids. Photography credits anti-clockwise from top right: O. Seehausen, O. Seehausen, O. Seehausen, J. Stroud, C. Martin, D. Pfennig, A. Hendry, R. Gillespie, K. Shaw, G. Bennett, E. Stacy, D. Rubinoff, J. Jeffreys, M. Knope, C. Parent, A. Hendry, J. Stroud, J. Mallet, P. Ryan, C. Wagner, C. Martin.

Figure 2.

Contrasting roles of: (1) factors external to the membership of the radiation coupled with divergent or disruptive selection associated with the environmental conditions or resource or host use; versus (2) reproductive incompatibility within the same environment fostering initial divergence, with ecological divergence, if it occurs, happening later and associated with interactions between relatives internal to the radiation. Part (1) is detailed further in Figure 3; part (2) in Figure 4.

Figure 3.

Entities formed by factors external to the radiation membership and associated with divergent or disruptive selection (building on Figure 2, part 1). The external environmental conditions and divergent or disruptive selection can lead to reproductive isolation between descendant lineages, owing to genotype by environment interactions. In some lineages, tighter co-occurrence can be achieved through character displacement in secondary contact.

Figure 4.

Entities formed by reproductive incompatibility within the same environment—separation in geographical space without any obvious divergent or disruptive selection (building on Figure 2, part 2). Ecological divergence may arise through interaction with close relatives within the radiation subsequent to the development of reproductive incompatibilities.

Figure 5.

Gene flow, traditionally considered to hinder divergence between incipient species, can serve to infuse variability that may foster adaptive radiation. This can take place through (a) hybrid origins of entire radiating clades (“hybrid swarm origins”) wherein admixture between one or more divergent lineages happens prior to the onset of radiation, (b) via hybridization between nonsister species within adaptive radiations that facilitates further speciation (“syngameon hypothesis”) (Seehausen 2004), and (c) speciation with gene flow between sister species. It is important to distinguish between how admixture is achieved in order to assess its effects on the process of adaptive radiation (Brock and Wagner 2018). Both syngameon and hybrid swarm origins hypotheses have now been well documented in cichlid fish (Meier et al. 2017), and the importance of gene flow and the syngameon have been well demonstrated in Heliconius butterflies (Mallet 2005; Merrill et al. 2015), as well as many plants (Barrier et al. 1999; Friar et al. 2008), and are also found in many other lineages (Feder et al. 2003; Lamichhaney et al. 2018). Indeed, the processes may be common to many adaptive radiations. Moreover, there may be a “sweet spot” in which divergent lineages can admix or hybridize and give rise to variability that is key to adaptive radiation.