What defines an adaptive radiation? Macroevolutionary diversification dynamics of an exceptionally species-rich continental lizard radiation
Daniel Pincheira-Donoso1*, Lilly P. Harvey1 and Marcello Ruta2
Daniel Pincheira-Donoso DPincheiraDonoso@lincoln.ac.uk
1 Laboratory of Evolutionary Ecology of Adaptations, School of Life Sciences, University of Lincoln, Brayford Campus, Lincoln LN6 7DL, UK
2 Laboratory of Evolutionary Palaeobiology, School of Life Sciences, University of Lincoln, Brayford Campus, Lincoln LN6 7DL, UK
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BMC Evolutionary Biology 2015, 15:153 doi:10.1186/s12862-015-0435-9
Received: 20 May 2015
Accepted: 29 July 2015
Published: 7 August 2015
© 2015 Pincheira-Donoso et al.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Adaptive radiation theory posits that ecological opportunity promotes rapid proliferation of phylogenetic and ecological diversity. Given that adaptive radiation proceeds via occupation of available niche space in newly accessed ecological zones, theory predicts that: (i) evolutionary diversification follows an ‘early-burst’ process, i.e., it accelerates early in the history of a clade (when available niche space facilitates speciation), and subsequently slows down as niche space becomes saturated by new species; and (ii) phylogenetic branching is accompanied by diversification of ecologically relevant phenotypic traits among newly evolving species. Here, we employ macroevolutionary phylogenetic model-selection analyses to address these two predictions about evolutionary diversification using one of the most exceptionally species-rich and ecologically diverse lineages of living vertebrates, the South American lizard genus Liolaemus.
Our phylogenetic analyses lend support to a density-dependent lineage diversification model. However, the lineage through-time diversification curve does not provide strong support for an early burst. In contrast, the evolution of phenotypic (body size) relative disparity is high, significantly different from a Brownian model during approximately the last 5 million years of Liolaemus evolution. Model-fitting analyses also reject the ‘early-burst’ model of phenotypic evolution, and instead favour stabilizing selection (Ornstein-Uhlenbeck, with three peaks identified) as the best model for body size diversification. Finally, diversification rates tend to increase with smaller body size.
Liolaemus have diversified under a density-dependent process with slightly pronounced apparent episodic pulses of lineage accumulation, which are compatible with the expected episodic ecological opportunity created by gradual uplifts of the Andes over the last ~25My. We argue that ecological opportunity can be strong and a crucial driver of adaptive radiations in continents, but may emerge less frequently (compared to islands) when major events (e.g., climatic, geographic) significantly modify environments. In contrast, body size diversification conforms to an Ornstein-Uhlenbeck model with multiple trait optima. Despite this asymmetric diversification between both lineages and phenotype, links are expected to exist between the two processes, as shown by our trait-dependent analyses of diversification. We finally suggest that the definition of adaptive radiation should not be conditioned by the existence of early-bursts of diversification, and should instead be generalized to lineages in which species and ecological diversity have evolved from a single ancestor.
Adaptive radiation theory predicts that the proliferation of phylogenetic and ecological diversity within a lineage results from the exposition of a single ancestor to multiple episodes of divergent natural selection , . A fundamental component of this process is the emergence of ‘ecological opportunity’, which provides the conditions that allow speciation through adaptation to different niches , . Ecological opportunity arises when spatial and/or ecological dispersal (i.e., access to novel niche dimensions facilitated by adaptive innovations) expose a species to a new set of abundant ecological resources –. For example, spatial and/or ecological dispersal can be driven by the emergence of new habitats (e.g., islands, mountains), by modifications of existing environments via climatic changes, or by the emptying of niches following extinctions –. As diversification proceeds, the extent of ecological opportunity declines as a function of increasing saturation of niche space by newly evolving species. Therefore, a core prediction based on the above scenario is that adaptively radiating lineages will show early bursts of rapid diversification followed by asymptotic decreases in diversification rates over time , –.
In addition, phenotypic traits with ecological significance play a fundamental role in the process of niche construction, and hence, in the way diversifying lineages saturate niches over time , . As a result, analyses of macroevolutionary models of lineage accumulation have been complemented with studies of tempo and mode of diversification of ecologically relevant phenotypes during adaptive radiations , , , . Based on the model of adaptively radiating lineages expounded above, we may predict that phenotypic diversification is high early in a group’s history, when ancestors enter an adaptive zone with abundant resources , . As natural selection promotes saturation of ecological space via phenotypic diversification, opportunities for niche occupation decline, thus causing a slowdown in the rates of diversification of ecologically functional traits , –. Consequently, if the radiation of a lineage has been adaptive, then the diversifications of both the lineage and the phenotype are expected to display similar patterns, which would be driven by changes in niche filling over time (e.g., , ). For instance, if the rapid early emergence of new species causes a decrease in niche space, then the opportunities for adaptive speciation decline, and slowdowns in ecological trait evolution would be expected given the reduced opportunities for adaptive niche expansions.
Evidence for coupled patterns of lineage and phenotype diversification is not consistent. While some studies reveal a link between these two components of diversity, others fail to identify such links. For example, Harmon et al.  showed that ‘bursts’ of lineage accumulation in the radiation of iguanian lizards are consistent with pulses of phenotypic disparity during their phylogenetic history. Similarly, the radiation of Caribbean Anolis lizards has been shown to partition ecological morphospace more finely as the numbers of competing lineages present on an island increase . In contrast, the radiation of cetaceans shows signals of diversity-dependent evolution of ecological phenotypes, while their net diversification fails to support a model of early-bursts of speciation followed by slowdowns . Finally, although net lineage diversification has been rapid and described by a diversity-dependent trajectory in the exceptionally explosive radiation of Rattus rats, the extent of interspecific morphological diversification has been minimal .
A number of hypotheses have been formulated to explain such disjoint patterns between lineage and phenotype diversity. For example, it has been suggested that the signatures of early burst adaptive radiations can be retained in phenotypic traits, while high extinction or fluctuations in net diversifications can erase them from the structure of the phylogeny , . Also, non-adaptive radiations are expected to diversify taxonomically but not much phenotypically , –. Finally, a longstanding debate focuses on whether macroevolutionary processes differ between island and continental radiations. Given that islands are spatially limited and have simpler ecological backgrounds compared to continents, both diversification processes and cladogenesis-phenotype links may follow different trajectories mediated by their intrinsic differences in ecological opportunity, which is expected to be more common on islands , –. In fact, although most biodiversity resides on continents , current knowledge on adaptive radiations derives primarily from island models. Therefore, studies of diversification dynamics in both lineages and phenotypes in continental radiations remain both a critical empirical and conceptual need and a promising research venue.
In recent years, the exceptionally diverse radiation of South American lizards of the genus Liolaemus has emerged as a promising model to investigate adaptiveradiations on continents. Consisting of 240+ species, Liolaemus is the world’s second richest genus of extant amniotes . Remarkably, since their origin (estimated ~22 Mya, , ), these lizards have adapted to the widest range of ecological and climatic conditions known among reptiles , , , , including extreme environments ranging from the Atacama Desert (the driest place on Earth) to Tierra del Fuego (the southernmost place where a reptile has been found), along both the Pacific and Atlantic coasts, and reaching up to 5,000 + m altitudes in the Andes , –. Importantly, recent studies suggest that this radiation may have been accelerated by the enormous ecological opportunity created by the Andes uplift , . This idea also suggests that the evolution of viviparity (live-bearing reproduction) provided the key innovation that unlocked the harsh Andean environments for early Liolaemus colonisation and subsequent diversification , , . Thus, this lineage offers a unique model to investigate the causes and trajectories of evolutionary radiations on continents. Here, we study the tempo and mode of macroevolutionary diversification in lineage richness and body size in the Liolaemus radiation, and discuss our findings in the context of radiations triggered by continental ecological opportunity. A central prediction derived from adaptive radiation theory is that both diversity dimensions will show signals of diversity-dependent diversification over time.
Our analyses are based on a multi-gene molecular, time-calibrated phylogenetic tree (Fig. 1), including 109 of the ~240 known Liolaemus species (the total number of species is difficult to determine given taxonomic controversies and the lack of reliable diagnoses for several species), extracted from Pyron et al.’s  comprehensive tree of squamates. The tree was time-calibrated using recent estimates obtained from molecular phylogenies of the major clades within Liolaemus, and based on the genus’ fossil record –. We set the origin of the Liolaemus crown group radiation (beginning with the latest common ancestry between the subgenera Eulaemus and Liolaemus sensu stricto) at 19.25 million years ago (Mya). This time represents the average between paleontological and molecular estimates, which place the origin of the crown group radiation, respectively, at 18.5 and 20 Mya.
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