Substitution rate variation among branches can lead to inaccurate reconstructions of evolutionary relationships and obscure the true phylogeny of affected clades. Body mass is often assumed to have a major influence on substitution rate, though other factors such as population size, life history traits, and flight demands are also thought to have an influence. Birds of the order Procellariiformes-which encompasses petrels, storm-petrels and albatrosses-show a striking 900-fold difference in body mass between the smallest and largest members, divergent life history traits, and substantial heterogeneity in mitochondrial substitution rates. Here, we used genome-scale nuclear DNA sequence data from 4365 ultraconserved element loci (UCEs) in 51 procellariiform species to examine whether phylogenetic reconstruction using genome-wide datasets is robust to the presence of rate heterogeneity, and to identify predictors of substitution rate variation. Our results provide a backbone phylogeny for procellariiform seabirds and resolve several controversies about the evolutionary history of the order, demonstrating that albatrosses are basal, storm-petrels are paraphyletic and diving petrels nestled within the Procellariidae. We find evidence of rate variation; however, all phylogenetic analyses using both concatenation and multispecies coalescent approaches recovered the same branching topology, including analyses implementing different clock models, and analyses of the most and least clock-like loci. Overall, we find that rate heterogeneity is little impacted by body mass, population size, age at first breeding, and longevity but moderately correlated with hand-wing index, a proxy for wing shape and flight efficiency. Given our results and the context of the broader literature perhaps it is time that we begin to question the prevailing paradigm that one or a few traits largely explain rate variation and accept instead that substitution rate may be the product of weak interactions among many, potentially taxon-specific, variables.
The "paradox of the great speciators" has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal ability to explain its occurrence on multiple islands, but reduced dispersal ability to explain its high number of subspecies. A rapid reduction in dispersal ability is often invoked to solve this apparent paradox, but a proximate mechanism has not been identified. Here, we explore the role of six genes linked to migration and animal personality differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, and SERT) in 20 South Pacific populations of silvereye (Zosterops lateralis) that range from highly sedentary to partially migratory, to determine if genetic variation is associated with dispersal propensity. We detected genetic associations in three of the six genes: i) in a partial migrant population, migrant individuals had longer microsatellite alleles at the CLOCK gene compared to resident individuals from the same population; ii) CREB1 displayed longer average microsatellite allele lengths in recently colonised island populations (< 200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction in CREB1 length with time since colonisation and decreasing dispersal propensity; and iii) like CREB1, DRD4 showed differences in polymorphisms between recent and old colonisations but a further sample size is needed to confirm. ADCYAP1, SERT, and NPAS2 were variable but that variation was not associated with dispersal propensity. The association of genetic variants at three genes with migration and dispersal ability in silvereyes provides the impetus for further exploration of genetic mechanisms underlying dispersal shifts, and the prospect of resolving a long-running evolutionary paradox through a genetic lens.
Parallel evolution occurs when the same trait evolves in closely related lineages in response to similar ecological contexts and provides some of the best examples of determinism in evolutionary biology. However, from a genetic standpoint, this process can be driven by either new mutations that appear independently in each diverging population or by selection on existing genetic variation common to both lineages. Small bodied birds, for example, tend to increase in size after they colonise a new island, following what is known as the 'island rule'. Such is the case of the Silvereye, a prolific natural coloniser of southwest Pacific islands. Island forms of this bird species increase in body size after they establish, with the pattern and pace of change consistent with directional natural selection and evident even in the most recent colonisations within the last 200 years. The system provides an exceptional opportunity to explore the genomic basis of repeated body size evolution. We sequenced 377 whole genomes from 31 different Silvereye populations, which revealed that both mechanisms are at play: in some lineages, new mutations are highly associated with body and bill size, but there are also highly associated polymorphisms present across all populations. Our research sheds light on the genomic basis of repeated body size evolution and emphasises that multiple molecular mechanisms can underlie similar evolutionary trajectories even within a single taxon.
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