Showing papers by "Daniel Ortiz-Barrientos published in 2019"

The origin and maintenance of metabolic allometry in animals.

Abstract: Organisms vary widely in size, from microbes weighing 0.1 pg to trees weighing thousands of megagrams — a 1021-fold range similar to the difference in mass between an elephant and the Earth. Mass has a pervasive influence on biological processes, but the effect is usually non-proportional; for example, a tenfold increase in mass is typically accompanied by just a four- to sevenfold increase in metabolic rate. Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns. We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds and mammals. We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time. The authors identify a strong positive relationship between mass and metabolic rate among insects, fish, amphibians, reptiles, birds and mammals, and show that the genetic and interspecific correlations between these traits are consistent with a pattern of multivariate selection.

Evidence for mutation-order speciation in an Australian wildflower

Abstract: In a number of animal species, divergent natural selection has repeatedly and independently driven the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation has evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also rapidly become new species. Mutation-order speciation, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.

Natural selection drives leaf divergence in experimental populations of Senecio lautus under natural conditions

Abstract: Leaf morphology is highly variable both within and between plant species. This study employs a combination of common garden and reciprocal transplant experiments to determine whether differences in leaf shape between ecotypes has evolved as an adaptive response to divergent ecological conditions.We created a synthetic population of hybrid genotypes to segregate morphological variation between three ecotypes and performed reciprocal transplants where this hybrid population was transplanted into the three adjacent native environments. We measured nine leaf morphology traits across the experimental and natural populations at these sites.We found significant divergence in multivariate leaf morphology toward the native character in each environment, suggesting environmental conditions at each site exert selective pressure that results in a phenotypic shift toward the local phenotype of the wild populations.These associations suggest that differences in leaf morphology between ecotypes have arisen as a result of divergent selection on leaf shape or associated traits that confer an adaptive advantage in each environment, which has led to the formation of morphologically distinct ecotypes.

Divergence in hormone signalling links local adaptation and hybrid failure

Abstract: Natural selection is a major driver for the origins of adaptations and new species. Whether or not the processes driving adaptation and speciation share a molecular basis remains largely unknown. Here, we show that divergence in hormone signalling contributed to the evolution of complex adaptations and intrinsic reproductive isolation in the Australian wildflower Senecio lautus. We provide evidence that differences in the auxin pathway, a hormone required for plant growth and development, has led to the repeated evolution of erect and prostrate forms along the Australian coast. Using multiple hybrid and natural populations, we show that adjacent erect and prostrate populations repeatedly diverged in auxin-related genes and auxin-dependent phenotypes, such as gravitropism. Analysis of a multi-year field selection experiment revealed that variation in fitness of an F10 hybrid population explained variation in gravitropism of their offspring. Genotyping of F11 hybrid individuals with extreme values of gravitropism revealed that variation in some of the most divergent genes explained both 65% of the variation in gravitropism and their probability of producing seed. Together, our results suggest that divergence in hormonal pathways can create a genetic link between rapid adaptation to new environments and the evolution of intrinsic reproductive isolation.

Evidence for mutation-order speciation between convergent ecotypes

Abstract: In a number of animal species, divergent natural selection repeatedly and independently drove the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments1. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare2. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also become new species rapidly. Mutation-order speciation2, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation, and is consistent with the increasingly common observation that there are multiple biochemical avenues to create convergent phenotypes. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.

Evidence for mutation-order speciation in Senecio lautus

Abstract: In a number of animal species, divergent natural selection has repeatedly and independently driven the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments1. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare2. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation has evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also rapidly become new species. Mutation-order speciation2, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.

Local adaptation and hybrid failure share a common genetic basis

Abstract: Testing whether local adaptation and intrinsic reproductive isolation share a genetic basis can reveal important connections between adaptation and speciation. Local adaptation arises as advantageous alleles spread through a population, but whether these same advantageous alleles fail on the genetic backgrounds of other populations remains largely unknown. We used a quantitative genetic breeding design to produce a late generation (F4) recombinant hybrid population by equally mating amongst four contrasting ecotypes of a native Australian daisy for four generations. We tracked fitness across generations and measured morphological traits in the glasshouse, and used a reciprocal transplant to quantify fitness in all four parental habitats. In the glasshouse, plants in the second generation showed a reduction in fitness as a loss of fertility, but this was fully recovered in the following generation. The F4 hybrid lacked extreme phenotypes present in the parental ecotypes, suggesting that genes reducing hybrid fitness were linked to traits specific to each ecotype. In the natural habitats, additive genetic variance for fitness was greatest for habitats that showed stronger native-ecotype advantage, suggesting that a loss of genetic variation present in the parental ecotypes were adaptive in the natural habitats. Reductions in genetic variance for fitness were associated with a loss of ecological trade-offs previously described in the parental ecotypes. Furthermore, natural selection on morphological traits differed amongst the parental habitats, but was not predicted to occur towards the morphology of the parental ecotypes. Together, these results suggest that intrinsic reproductive isolation removed adaptive genetic variation present in the parental ecotypes. The evolution of these distinct ecotypes was likely governed by genetic variation that resulted in both ecological trade-offs and intrinsic reproductive isolation among populations adapted to contrasting environments.

Connecting micro and macroevolution using genetic incompatibilities and natural selection on additive genetic variance

Abstract: Evolutionary biologists have long sought to identify the links between micro and macroevolution to better understand how biodiversity is created. Despite the pursuit, it remains a challenge to understand how allele frequency changes correlate with the evolution of morphological diversity, and the build-up of reproductive isolation. To connect micro and macroevolution, we tested the adaptive importance of alleles underlying genetic incompatibilities, and the consequences for predicting evolutionary trajectories. Using a quantitative genetics crossing design, we produced an F4 Advanced Recombinant Form (ARF) between four contrasting ecotypes, which we phenotyped in the glasshouse (N=770) and transplanted into the four natural habitats (N=14,265 seeds), alongside the parental ecotypes. F2 hybrid breakdown was associated with the loss of extreme phenotypes and environment-specific genetic variation in field performance. We found evidence of genetic trade-offs among environments, but only in axes describing smaller amounts of genetic variance for fitness. Habitats that showed stronger patterns of adaptive divergence for native versus foreign ecotypes, also showed lower genetic variance in fitness of the ARF. Integrating data from the field and glasshouse predicted patterns of selection on morphological traits in a similar direction to the parental ecotypes. Overall, our results provide strong empirical evidence linking ecotype specific alleles with fitness trade-offs, phenotypic divergence and the rise in genetic incompatibilities among recently derived ecotypes. Our data connects microevolutionary change with macroevolution through adaptive radiation, where increases in environment specific alleles create changes in the distribution of genetic variance, ameliorating genetic constraints to adaptation as adaptive divergence proceeds.