The genetics of evolutionary radiations

With the realization that much of the biological diversity on Earth has been generated by discrete evolutionary radiations, there has been a rapid increase in research into the biotic (key innovations) and abiotic (key environments) circumstances in which such radiations took place. Here we focus on the potential importance of population genetic structure and trait genetic architecture in explaining radiations. We propose a verbal model describing the stages of an evolutionary radiation: first invading a suitable adaptive zone and expanding both spatially and ecologically through this zone; secondly, diverging genetically into numerous distinct populations; and, finally, speciating. There are numerous examples of the first stage; the difficulty, however, is explaining how genetic diversification can take place from the establishment of a, presumably, genetically depauperate population in a new adaptive zone. We explore the potential roles of epigenetics and transposable elements (TEs), of neutral process such as genetic drift in combination with trait genetic architecture, of gene flow limitation through isolation by distance (IBD), isolation by ecology and isolation by colonization, the possible role of intra‐specific competition, and that of admixture and hybridization in increasing the genetic diversity of the founding populations. We show that many of the predictions of this model are corroborated. Most radiations occur in complex adaptive zones, which facilitate the establishment of many small populations exposed to genetic drift and divergent selection. We also show that many radiations (especially those resulting from long‐distance dispersal) were established by polyploid lineages, and that many radiating lineages have small genome sizes. However, there are several other predictions which are not (yet) possible to test: that epigenetics has played a role in radiations, that radiations occur more frequently in clades with small gene flow distances, or that the ancestors of radiations had large fundamental niches. At least some of these may be testable in the future as more genome and epigenome data become available. The implication of this model is that many radiations may be hard polytomies because the genetic divergence leading to speciation happens within a very short time, and that the divergence history may be further obscured by hybridization. Furthermore, it suggests that only lineages with the appropriate genetic architecture will be able to radiate, and that such a radiation will happen in a meta‐population environment. Understanding the genetic architecture of a lineage may be an essential part of accounting for why some lineages radiate, and some do not.     

The skull evolution of oviraptorosaurian dinosaurs: the role of niche partitioning in diversification

Oviraptorosaurs are bird‐like theropod dinosaurs that thrived in the final pre‐extinction ecosystems during the latest Cretaceous, and the beaked, toothless skulls of derived species are regarded as some of the most peculiar among dinosaurs. Their aberrant morphologies are hypothesized to have been caused by rapid evolution triggered by an ecological/biological driver, but little is known about how their skull shapes and functional abilities diversified. Here, we use quantitative techniques to study oviraptorosaur skull form and mandibular function. We demonstrate that the snout is particularly variable, that mandibular form and upper/lower beak form are significantly correlated with phylogeny, and that there is a strong and significant correlation between mandibular function and mandible/lower beak shape, suggesting a form–function association. The form–function relationship and phylogenetic signals, along with a moderate allometric signal in lower beak form, indicate that similar mechanisms governed beak shape in oviraptorosaurs and extant birds. The two derived oviraptorosaur clades, oviraptorids and caenagnathids, are significantly separated in morphospace and functional space, indicating that they partitioned niches. Oviraptorids coexisting in the same ecosystem are also widely spread in morphological and functional space, suggesting that they finely partitioned feeding niches, whereas caenagnathids exhibit extreme disparity in beak size. The diversity of skull form and function was likely key to the diversification and evolutionary success of oviraptorosaurs in the latest Cretaceous.     

Resource diversity promotes among‐individual diet variation,but not genomic diversity,in lake stickleback

Many generalist species consist of specialised individuals that use different resources. This within‐population niche variation can stabilise population and community dynamics. Consequently, ecologists wish to identify environmental settings that promote such variation. Theory predicts that environments with greater resource diversity favour ecological diversity among consumers (via disruptive selection or plasticity). Alternatively, niche variation might be a side‐effect of neutral genomic diversity in larger populations. We tested these alternatives in a metapopulation of threespine stickleback. Stickleback consume benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate‐sized lakes support generalist stickleback populations using an even mixture of the two prey types, and exhibit greater among‐individual variation in diet and morphology. In contrast, genomic diversity increases with lake size. Thus, phenotypic diversity and neutral genetic polymorphism are decoupled: trophic diversity being greatest in intermediate‐sized lakes with high resource diversity, whereas neutral genetic diversity is greatest in the largest lakes.     

石山苣苔属四种(含一变种)植物的染色体数目和倍性研究

石山苣苔属(苦苣苔科)约41种,主要分布于我国西南石灰岩地区。到目前为止,仅其中四种的染色体数目被研究和报道,其余绝大多数物种的染色体数目和倍性尚不清楚,染色体数目和倍性在该属及其姐妹属报春苣苔属中的演变历史及其对两属物种多样性分化的影响亦不清楚。该文以叶片水培生根法获取的四种(含一变种)石山苣苔属植物 [即石山苣苔原变种(Petrocodon dealbatus var. dealbatus)、齿缘石山苣苔(Petrocodon dealbatus var. denticulatus)、弄岗石山苣苔(Petrocodon longangensis)、石山苣苔未定名种(Petrocodon sp.)]的根尖细胞为材料开展染色体实验,探索了多种不同的实验条件对染色体制片效果的影响并获取染色体数目,在石山苣苔属和报春苣苔属的系统树上追踪了染色体数目和倍性的演变历史,同时探讨染色体数目尤其是倍性变化是否对两属物种多样性分化存在影响。结果表明:(1)长度为1～1.5 cm的根尖,0.002 mol·L^-1 8-羟基喹啉溶液预处理5 h,解离4 min为较适宜的染色体制备条件。(2)四种(含一变种)石山苣苔属植物染色体数目一致,均为二倍体(2n=2x=36)。(3)两属之间及两属各自的最近共同祖先染色体数目尚不能确定,除个别物种染色体条数或倍性有变化以外,其余已知染色体数目的物种均为2n=2x=36,在两属中高度一致,石山苣苔属与报春苣苔属物种多样性分化尤其两属物种多样性巨大差异与染色体数目和基因组倍性变化无关。综上结果为石山苣苔属植物及其近缘类群染色体制备提供了参考,也为进一步对该类群的分类、系统演化和物种形成等方面的研究提供了基础数据和启示。     

The signature of competition in ecomorphological traits across the avian radiation

Competition for shared resources represents a fundamental driver of biological diversity. However, the tempo and mode of phenotypic evolution in deep-time has been predominantly investigated using trait evolutionary models which assume that lineages evolve independently from each other. Consequently, the role of species interactions in driving macroevolutionary dynamics remains poorly understood. Here, we quantify the prevalence for signatures of competition between related species in the evolution of ecomorphological traits across the bird radiation. We find that mechanistic trait models accounting for the effect of species interactions on phenotypic divergence provide the best fit for the data on at least one trait axis in 27 out of 59 clades ranging between 21 and 195 species. Where it occurs, the signature of competition generally coincides with positive species diversity-dependence, driven by the accumulation of lineages with similar ecologies, and we find scarce evidence for trait-dependent or negative diversity-dependent phenotypic evolution. Overall, our results suggest that the footprint of interspecific competition is often eroded in long-term patterns of phenotypic diversification, and that other selection pressures may predominantly shape ecomorphological diversity among extant species at macroevolutionary scales.     

“Into and Out of” the Qinghai‐Tibet Plateau and the Himalayas: Centers of origin and diversification across five clades of Eurasian montane and alpine passerine birds

Encompassing some of the major hotspots of biodiversity on Earth, large mountain systems have long held the attention of evolutionary biologists. The region of the Qinghai‐Tibet Plateau (QTP) is considered a biogeographic source for multiple colonization events into adjacent areas including the northern Palearctic. The faunal exchange between the QTP and adjacent regions could thus represent a one‐way street (“out of” the QTP). However, immigration into the QTP region has so far received only little attention, despite its potential to shape faunal and floral communities of the QTP. In this study, we investigated centers of origin and dispersal routes between the QTP, its forested margins and adjacent regions for five clades of alpine and montane birds of the passerine superfamily Passeroidea. We performed an ancestral area reconstruction using BioGeoBEARS and inferred a time‐calibrated backbone phylogeny for 279 taxa of Passeroidea. The oldest endemic species of the QTP was dated to the early Miocene (ca. 20 Ma). Several additional QTP endemics evolved in the mid to late Miocene (12–7 Ma). The inferred centers of origin and diversification for some of our target clades matched the “out of Tibet hypothesis’ or the “out of Himalayas hypothesis” for others they matched the “into Tibet hypothesis.” Three radiations included multiple independent Pleistocene colonization events to regions as distant as the Western Palearctic and the Nearctic. We conclude that faunal exchange between the QTP and adjacent regions was bidirectional through time, and the QTP region has thus harbored both centers of diversification and centers of immigration.     

Evolutionary trajectory of fish Piscine novirhabdovirus (=Viral Hemorrhagic Septicemia Virus) across its Laurentian Great Lakes history: Spatial and temporal diversification

Piscine novirhabdovirus = Viral Hemorrhagic Septicemia Virus (VHSV) first appeared in the Laurentian Great Lakes with large outbreaks from 2005 to 2006, as a new and novel RNA rhabdovirus subgenogroup (IVb) that killed >30 fish species. Interlude periods punctuated smaller more localized outbreaks in 2007, 2010, and 2017, although some fishes tested positive in the intervals. There have not been reports of outbreaks or positives from 2018, 2019, or 2020. Here, we employ a combined population genetics and phylogenetic approach to evaluate spatial and temporal evolutionary trajectory on its G‐gene sequence variation, in comparison with whole‐genome sequences (11,083 bp) from a subset of 44 individual isolates (including 40 newly sequenced ones). Our results show that IVb (N = 184 individual fish isolates) diversified into 36 G‐gene haplotypes from 2003 to 2017, stemming from two originals (“a” and “b”). G‐gene haplotypes “a” and “b” differed by just one synonymous single‐nucleotide polymorphism (SNP) substitution, remained the most abundant until 2011, then disappeared. Group “a” descendants (14 haplotypes) remained most prevalent in the Upper and Central Great Lakes, with eight (51%) having nonsynonymous substitutions. Group “b” descendants primarily have occurred in the Lower Great Lakes, including 22 haplotypes, of which 15 (68%) contained nonsynonymous changes. Evolutionary patterns of the whole‐genome sequences (which had 34 haplotypes among 44 isolates) appear congruent with those from the G‐gene. Virus populations significantly diverged among the Upper, Central, and Lower Great Lakes, diversifying over time. Spatial divergence was apparent in the overall patterns of nucleotide substitutions, while amino acid changes increased temporally. VHSV‐IVb thus significantly differentiated across its less than two decades in the Great Lakes, accompanied by declining outbreaks and virulence. Continuing diversification likely allowed the virus to persist at low levels in resident fish populations, and may facilitate its potential for further and future spread to new habitats and nonacclimated hosts.     

Ecological and morphological determinants of evolutionary diversification in Darwin's finches and their relatives

Darwin''s finches are a classic example of adaptive radiation, a process by which multiple ecologically distinct species rapidly evolve from a single ancestor. Such evolutionary diversification is typically explained by adaptation to new ecological opportunities. However, the ecological diversification of Darwin''s finches following their dispersal to Galápagos was not matched on the same archipelago by other lineages of colonizing land birds, which diversified very little in terms of both species number and morphology. To better understand the causes underlying the extraordinary variation in Darwin''s finches, we analyze the evolutionary dynamics of speciation and trait diversification in Thraupidae, including Coerebinae (Darwin''s finches and relatives) and, their closely related clade, Sporophilinae. For all traits, we observe an early pulse of speciation and morphological diversification followed by prolonged periods of slower steady‐state rates of change. The primary exception is the apparent recent increase in diversification rate in Darwin''s finches coupled with highly variable beak morphology, a potential key factor explaining this adaptive radiation. Our observations illustrate how the exploitation of ecological opportunity by contrasting means can produce clades with similarly high diversification rate yet strikingly different degrees of ecological and morphological differentiation.     

Environmentally induced phenotypic plasticity and DNA methylation changes in a wild potato growing in two contrasting Andean experimental gardens

DNA methylation can be environmentally modulated and plays a role in phenotypic plasticity. To understand the role of environmentally induced epigenetic variation and its dynamics in natural populations and ecosystems, it is relevant to place studies in a real-world context. Our experimental model is the wild potato Solanum kurtzianum, a close relative of the cultivated potato S. tuberosum. It was evaluated in its natural habitat, an arid Andean region in Argentina characterised by spatial and temporal environmental fluctuations. The dynamics of phenotypic and epigenetic variability (with Methyl Sensitive Amplified Polymorphism markers, MSAP) were assayed in three genotypes across three growing seasons. These genotypes were cultivated permanently and also reciprocally transplanted between experimental gardens (EG) differing in ca. 1000 m of altitude. In two seasons, the genotypes presented differential methylation patterns associated to the EG. In the reciprocal transplants, a rapid epigenomic remodelling occurred according to the growing season. Phenotypic plasticity, both spatial (between EGs within season) and temporal (between seasons), was detected. The epigenetic and phenotypic variability was positively correlated. The lack of an evident mitotic epigenetic memory would be a common response to short-term environmental fluctuations. Thus, the environmentally induced phenotypic and epigenetic variation could contribute to populations persistence through time. These results have implications for understanding the great ecological diversity of wild potatoes.