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- Journal of Heredity
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Alba, Mar (Ed.)Abstract Adaptive radiations are characterised by the diversification and ecological differentiation of species, and replicated cases of this process provide natural experiments for understanding the repeatability and pace of molecular evolution. During adaptive radiation, genes related to ecological specialisation may be subject to recurrent positive directional selection. However, it is not clear to what extent patterns of lineage-specific ecological specialisation (including phenotypic convergence) are correlated with shared signatures of molecular evolution. To test this, we sequenced whole exomes from a phylogenetically dispersed sample of 38 murine rodent species, a group characterised by multiple, nested adaptive radiations comprising extensive ecological and phenotypic diversity. We found that genes associated with immunity, reproduction, diet, digestion and taste have been subject to pervasive positive selection during the diversification of murine rodents. We also found a significant correlation between genome-wide positive selection and dietary specialisation, with a higher proportion of positively selected codon sites in derived dietary forms (i.e. carnivores and herbivores) than in ancestral forms (i.e. omnivores). Despite striking convergent evolution of skull morphology and dentition in two distantly related worm-eating specialists, we did not detect more genes with shared signatures of positive or relaxed selection than in a non-convergent species comparison. While a small number of the genes we detected can be incidentally linked to craniofacial morphology or diet, protein-coding regions are unlikely to be the primary genetic basis of this complex convergent phenotype. Our results suggest a link between positive selection and derived ecological phenotypes, and highlight specific genes and general functional categories that may have played an integral role in the extensive and rapid diversification of murine rodents.more » « less
To determine the historical dynamics of colonization and whether the relative timing of colonization predicts diversification rate in the species‐rich, murine rodent communities of Indo‐Australia.
Indo‐Australian Archipelago including the Sunda shelf of continental Asia, Sahul shelf of continental Australia, the Philippines and Wallacea of Indonesia.
Order Rodentia, Family Muridae.
We used a fossil‐calibrated molecular phylogeny and Bayesian biogeographical modelling to infer the frequency and temporal sequence of biogeographical transitions among Sunda, Sahul, the Philippines and Wallacea. We estimated diversification rates for each colonizing lineage using a method‐of‐moments estimator of net diversification and Bayesian mixture model estimates of diversification rate shifts.
We identified 17 biogeographical transitions, including nine originating from Sunda, seven originating from Sulawesi and broader Wallacea and one originating from Sahul. Wallacea was colonized eight times, the Phillipines five times, Sunda twice and Sahul twice. Net diversification rates ranged from 0.2 to 2.12 species/lineage/My with higher rates in secondary and later colonizers than primary colonizers. The highest rates were in the genus
Rattusand their closest relatives, irrespective of colonization history. Main Conclusions
Our inferences from murines demonstrate once again the substantial role of islands as sources of species diversity in terrestrial vertebrates of the IAA with most speciation events occurring on islands. Sulawesi and broader Wallacea have been a major source of colonists for both island and continental systems. Crossings of Wallace's Line were more common than subsequent transitions across Lydekker's Line to the east. While speciation following colonization of oceanic archipelagos and large islands is consistent with adaptive radiation theory and ideas regarding ecological opportunity, we did not observe a strong signal of incumbency effects. Rather, subsequent colonists of landmasses radiated unhindered by previous radiations.
Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting diﬀerent host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic eﬀects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R. cingulata group.more » « less
Rapid adaptive radiation poses a distinct question apart from speciation and adaptation: what happens after one speciation event? That is, how are some lineages able to continue speciating through a rapid burst? This question connects global macroevolutionary patterns to microevolutionary processes. Here we review major features of rapid radiations in nature and their mismatch with theoretical models and what is currently known about speciation mechanisms. Rapid radiations occur on three major diversification axes – species richness, phenotypic disparity, and ecological diversity – with exceptional outliers on each axis. The paradox is that the hallmark early stage of adaptive radiation, a rapid burst of speciation and niche diversification, is contradicted by most existing speciation models which instead predict continuously decelerating speciation rates and niche subdivision through time. Furthermore, while speciation mechanisms such as magic traits, phenotype matching, and physical linkage of co-adapted alleles promote speciation, it is often not discussed how these mechanisms could promote multiple speciation events in rapid succession. Additional mechanisms beyond ecological opportunity are needed to understand how rapid radiations occur. We review the evidence for five emerging theories: 1) the ‘transporter’ hypothesis: introgression and the ancient origins of adaptive alleles, 2) the ‘signal complexity’ hypothesis: the dimensionality of sexual traits, 3) the connectivity of fitness landscapes, 4) ‘diversity begets diversity’, and 5) flexible stem/‘plasticity first’. We propose new questions and predictions to guide future work on the mechanisms underlying the rare origins of rapid radiation.more » « less
There are multiple hypotheses for the spectacular plant diversity found in deserts. We explore how different factors, including the roles of ecological opportunity and selection, promote diversification and disparification in
Encelia, a lineage of woody plants in the deserts of the Americas.
Using a nearly complete species‐level phylogeny based on double‐digest restriction‐aided sequencing along with a broad set of phenotypic traits, we estimate divergence times and diversification rates, identify instances of hybridization, quantify trait disparity and assess phenotypic divergence across environmental gradients.
We show that
Enceliaoriginated and diversified recently (mid‐Pleistocene) and rapidly, with rates comparable to notable adaptive radiations in plants. Enceliaprobably originated in the hot deserts of North America, with subsequent diversification across steep environmental gradients. We uncover multiple instances of gene flow between species. The radiation of Enceliais characterized by fast rates of phenotypic evolution, trait lability and extreme disparity across environments and between species pairs with overlapping geographic ranges. Enceliaexemplifies how interspecific gene flow in combination with high trait lability can enable exceptionally fast diversification and disparification across steep environmental gradients.