Macroevolutionary diversification with limited niche disparity in a species-rich lineage of cold-climate lizards

Abstract

BackgroundLife diversifies via adaptive radiation when natural selection drives the evolution of ecologically distinct species mediated by their access to novel niche space, or via non-adaptive radiation when new species diversify while retaining ancestral niches. However, while cases of adaptive radiation are widely documented, examples of non-adaptively radiating lineages remain rarely observed. A prolific cold-climate lizard radiation from South America (Phymaturus), sister to a hyper-diverse adaptive radiation (Liolaemus), has extensively diversified phylogenetically and geographically, but with exceptionally minimal ecological and life-history diversification. This lineage, therefore, may offer unique opportunities to investigate the non-adaptive basis of diversification, and in combination with Liolaemus, to cover the whole spectrum of modes of diversification predicted by theory, from adaptive to non-adaptive. Using phylogenetic macroevolutionary modelling performed on a newly created 58-species molecular tree, we establish the tempo and mode of diversification in the Phymaturus radiation.ResultsLineage accumulation in Phymaturus opposes a density-dependent (or ‘niche-filling’) process of diversification. Concurrently, we found that body size diversification is better described by an Ornstein-Uhlenbeck evolutionary model, suggesting stabilizing selection as the mechanism underlying niche conservatism (i.e., maintaining two fundamental size peaks), and which has predominantly evolved around two major adaptive peaks on a ‘Simpsonian’ adaptive landscape.ConclusionsLineage diversification of the Phymaturus genus does not conform to an adaptive radiation, as it is characterised by a constant rate of species accumulation during the clade’s history. Their strict habitat requirements (rocky outcrops), predominantly invariant herbivory, and especially the constant viviparous reproduction across species have likely limited their opportunities for adaptive diversifications throughout novel environments. This mode of diversification contrasts dramatically with its sister lineage Liolaemus, which geographically overlaps with Phymaturus, but exploits all possible microhabitats in these and other bioclimatic areas. Our study contributes importantly to consolidate these lizards (liolaemids) as promising model systems to investigate the entire spectrum of modes of species formations, from the adaptive to the non-adaptive extremes of the continuum.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1133-1) contains supplementary material, which is available to authorized users.

How important is it to consider lineage diversification heterogeneity in macroevolutionary studies? Lessons from the lizard family Liolaemidae

“…Specialization in Phymaturus has been discussed in other studies (e.g. Marín‐Gonzalez, Olave, Avila, Sites, & Morando, ; Olave et al, in press; Reaney, Saldarriaga‐Córdoba, & Pincheira‐Donoso, ); specialization may be advantageous if it results in efficient selection for adaptation to a stable and narrow niche, reducing the cost of trade‐offs by abandoning traits needed to utilize a wider range of resources (Futuyma & Moreno, ). However, these shorter‐term microevolutionary benefits may come at the cost of longer‐term macroevolutionary success (e.g.…”

How important is it to consider lineage diversification heterogeneity in in macroevolutionary studies: lessons from the lizard family Liolaemidae

“…Specialization in Phymaturus has been discussed in other studies (e.g. Reaney et al 2018;Marín-Gonzalez et al 2018;Olave et al in press); specialization may be advantageous if it results in efficient selection for adaptation to a stable and narrow niche, reducing the cost of trade-offs by abandoning traits needed to utilize a wider range of resources (Futuyma and Moreno 1988). However, these shorter term microevolutionary benefits may come at the cost of longer term macroevolutionary success (e.g.…”

Live fast, diversify non-adaptively: evolutionary diversification of exceptionally short-lived annual killifishes

“…During this process of non-adaptive radiation [15], episodes of speciation are not the result of divergent natural selection and thus, newly emerging species remain ecologically and phenotypically similar [16]. Importantly, it has been suggested that in contrast to adaptive radiations, diversification via non-adaptive radiation is more likely to take place when newly emerging species radiate across geographically non-overlapping areas (allopatry), which can accommodate species with fundamentally similar niche demands [15, 17, 18]. The availability of such areas equipped with suitable ‘ancestral’ ecological conditions is what we refer to as ‘spatial opportunity’.…”

“…Given that this form of radiation is bound by the availability of spatial opportunity, rather than by environments with an abundance of diverse niche space, the process of species accumulation is not expected to always exhibit a slow-down over time. Instead, an arithmetic accumulation of species is expected when incipient species encounter new spatial opportunity to continue clade expansion producing a phylogenetic late-burst [18]. Alternatively, if an abundance of spatial opportunity is available and exploited early in the clades’ history, it will produce an early burst, akin to an adaptive radiation [8].…”

“…The fundamental principles underlying non-adaptive radiations are well-studied ([24] and references therein). In contrast, the phylogenetic characterisation of the tempo and mode of non-adaptive radiations has emerged more recently and remains a pending task in our understanding of the role of adaptation during diversification [8, 18, 25, 26]. The extent to which niche and phenotypic disparity are preserved across prolific clades, and the impact of coexistence among some of the species to exert a triggering phenomenon such as ecological character displacement remain poorly known.…”