Realized evolvability: quantifying phenotypic evolution in a Drosophila clade

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)

Phenotypic evolution in a fossil gastropod species lineage: evidence for adaptive radiation?

Detecting speciation in the fossil record is a particularly challenging matter. Palaeontologists are usually confronted with poor preservation and limited knowledge on the palaeoenvironment. Even in the contrary case of adequate preservation and information, the linkage of pattern to process is often obscured by insufficient temporal resolution. Consequently, reliable documentations of speciation in fossils with discussions on underlying mechanisms are rare. Here we present a well-resolved pattern of morphological evolution in a fossil species lineage of the gastropod Melanopsis in the long-lived Lake Pannon. These developments are related to environmental changes, documented by isotope and stratigraphical data. After a long period of stasis, the ancestral species experiences a phenotypic change expressed as shift and expansion of the morphospace. The appearance of several new phenotypes along with changes in the environment is interpreted as adaptive radiation. Lake-level high stands affect distribution and availability of habitats and, as a result of varied functional demands on shell geometry, the distribution of phenotypes. The on-going divergence of the morphospace into two branches argues for increasing reproductive isolation, consistent with the model of ecological speciation. In the latest phase, however, progressively unstable conditions restrict availability of niches, allowing survival of one branch only.

Phenotypic evolution in a venerid bivalve species lineage from the late Middle Miocene Central Paratethys Sea: a multi-approach morphometric analysis

A morphometric analysis was performed for the late Middle Miocene bivalve species lineage of Polititapes tricuspis (Eichwald, 1829) (Veneridae: Tapetini). Specimens from various localities grouped into two stratigraphically successive biozones, i.e. the upper Ervilia Zone and the Sarmatimactra Zone, were investigated using a multi-method approach. A Generalized Procrustes Analysis was computed for fifteen landmarks, covering characteristics of the hinge, muscle scars, and pallial line. The shell outline was separately quantified by applying the Fast Fourier Transform, which redraws the outline by fitting in a combination of trigonometric curves. Shell size was calculated as centroid size from the landmark configuration. Shell thickness, as not covered by either analysis, was additionally measured at the centroid. The analyses showed significant phenotypic differentiation between specimens from the two biozones. The bivalves become distinctly larger and thicker over geological time and develop circular shells with stronger cardinal teeth and a deeper pallial sinus. Data on the paleoenvironmental changes in the late Middle Miocene Central Paratethys Sea suggest the phenotypic shifts to be functional adaptations. The typical habitats for Polititapes changed to extensive, very shallow shores exposed to high wave action and tidal activity. Caused by the growing need for higher mechanical stability, the bivalves produced larger and thicker shells with stronger cardinal teeth. The latter are additionally shifted towards the hinge center to compensate for the lacking lateral teeth and improve stability. The deepening pallial sinus is related to a deeper burrowing habit, which is considered to impede being washed out in the new high-energy settings.

Studying phenotypic evolution using multivariate quantitative genetics

Quantitative genetics provides a powerful framework for studying phenotypic evolution and the evolution of adaptive genetic variation. Central to the approach is G, the matrix of additive genetic variances and covariances. G summarizes the genetic basis of the traits and can be used to predict the phenotypic response to multivariate selection or to drift. Recent analytical and computational advances have improved both the power and the accessibility of the necessary multivariate statistics. It is now possible to study the relationships between G and other evolutionary parameters, such as those describing the mutational input, the shape and orientation of the adaptive landscape, and the phenotypic divergence among populations. At the same time, we are moving towards a greater understanding of how the genetic variation summarized by G evolves. Computer simulations of the evolution of G, innovations in matrix comparison methods, and rapid development of powerful molecular genetic tools have all opened the way for dissecting the interaction between allelic variation and evolutionary process. Here I discuss some current uses of G, problems with the application of these approaches, and identify avenues for future research.

Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton

Marine phytoplankton can evolve rapidly when confronted with aspects of climate change because of their large population sizes and fast generation times. Despite this, the importance of environment fluctuations, a key feature of climate change, has received little attention-selection experiments with marine phytoplankton are usually carried out in stable environments and use single or few representatives of a species, genus or functional group. Here we investigate whether and by how much environmental fluctuations contribute to changes in ecologically important phytoplankton traits such as C:N ratios and cell size, and test the variability of changes in these traits within the globally distributed species Ostreococcus. We have evolved 16 physiologically distinct lineages of Ostreococcus at stable high CO2 (1031±87?µatm CO2, SH) and fluctuating high CO2 (1012±244?µatm CO2, FH) for 400 generations. We find that although both fluctuation and high CO2 drive evolution, FH-evolved lineages are smaller, have reduced C:N ratios and respond more strongly to further increases in CO2 than do SH-evolved lineages. This indicates that environmental fluctuations are an important factor to consider when predicting how the characteristics of future phytoplankton populations will have an impact on biogeochemical cycles and higher trophic levels in marine food webs.

The Roles of Phenotypic Plasticity and Plant-Microbe Interactions in the Evolution of Complex Traits in Boechera stricta

All organisms live in complex habitats that shape the course of their evolution by altering the phenotype expressed by a given genotype (a phenomenon known as phenotypic plasticity) and simultaneously by determining the evolutionary fitness of that phenotype. In some cases, phenotypic evolution may alter the environment experienced by future generations. This dissertation describes how genetic and environmental variation act synergistically to affect the evolution of glucosinolate defensive chemistry and flowering time in Boechera stricta, a wild perennial herb. I focus particularly on plant-associated microbes as a part of the plant’s environment that may alter trait evolution and in turn be affected by the evolution of those traits. In the first chapter I measure glucosinolate production and reproductive fitness of over 1,500 plants grown in common gardens in four diverse natural habitats, to describe how patterns of plasticity and natural selection intersect and may influence glucosinolate evolution. I detected extensive genetic variation for glucosinolate plasticity and determined that plasticity may aid colonization of new habitats by moving phenotypes in the same direction as natural selection. In the second chapter I conduct a greenhouse experiment to test whether naturally-occurring soil microbial communities contributed to the differences in phenotype and selection that I observed in the field experiment. I found that soil microbes cause plasticity of flowering time but not glucosinolate production, and that they may contribute to natural selection on both traits; thus, non-pathogenic plant-associated microbes are an environmental feature that could shape plant evolution. In the third chapter, I combine a multi-year, multi-habitat field experiment with high-throughput amplicon sequencing to determine whether B. stricta-associated microbial communities are shaped by plant genetic variation. I found that plant genotype predicts the diversity and composition of leaf-dwelling bacterial communities, but not root-associated bacterial communities. Furthermore, patterns of host genetic control over associated bacteria were largely site-dependent, indicating an important role for genotype-by-environment interactions in microbiome assembly. Together, my results suggest that soil microbes influence the evolution of plant functional traits and, because they are sensitive to plant genetic variation, this trait evolution may alter the microbial neighborhood of future B. stricta generations. Complex patterns of plasticity, selection, and symbiosis in natural habitats may impact the evolution of glucosinolate profiles in Boechera stricta.

Adaptive evolution of four microcephaly genes and the evolution of brain size in anthropoid primates

The anatomical basis and adaptive function of the expansion in primate brain size have long been studied; however, we are only beginning to understand the genetic basis of these evolutionary changes. Genes linked to human primary microcephaly have received much attention as they have accelerated evolutionary rates along lineages leading to humans. However, these studies focus narrowly on apes, and the link between microcephaly gene evolution and brain evolution is disputed. We analyzed the molecular evolution of four genes associated with microcephaly (ASPM, CDK5RAP2, CENPJ, MCPH1) across 21 species representing all major clades of anthropoid primates. Contrary to prevailing assumptions, positive selection was not limited to or intensified along the lineage leading to humans. In fact we show that all four loci were subject to positive selection across the anthropoid primate phylogeny. We developed clearly defined hypotheses to explicitly test if selection on these loci was associated with the evolution of brain size. We found positive relationships between both CDK5RAP2 and ASPM and neonatal brain mass and somewhat weaker relationships between these genes and adult brain size. In contrast, there is no evidence linking CENPJ and MCPH1 to brain size evolution. The stronger association of ASPM and CDK5RAP2 evolution with neonatal brain size than with adult brain size is consistent with these loci having a direct effect on prenatal neuronal proliferation. These results suggest that primate brain size may have at least a partially conserved genetic basis. Our results contradict a previous study that linked adaptive evolution of ASPM to changes in relative cortex size; however, our analysis indicates that this conclusion is not robust. Our finding that the coding regions of two widely expressed loci has experienced pervasive positive selection in relation to a complex, quantitative developmental phenotype provides a notable counterexample to the commonly asserted hypothesis that cisregulatory regions play a dominant role in phenotypic evolution. Key words: ASPM, MCPH1, CDK5RAP2, CENPJ, brain, neurogenesis, primates.

Effects of allometry, productivity and lifestyle on rates and limits of body size evolution

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

Positive phenotypic selection inferred from phylogenies

Rates of phenotypic evolution vary widely in nature and these rates may often reflect the intensity of natural selection. Here we outline an approach for detecting exceptional shifts in the rate of phenotypic evolution across phylogenies. We introduce a simple new branch-specific metric ∆V/∆B that divides observed phenotypic change along a branch into two components: (1) that attributable to the background rate (∆B), and (2) that attributable to departures from the background rate (∆V). Where the amount of expected change derived from variation in the rate of morphological evolution doubles that explained by to the background rate (∆V/∆B > 2), we identify this as positive phenotypic selection. We apply our approach to six datasets, finding multiple instances of positive selection in each. Our results support the growing appreciation that the traditional gradual view of phenotypic evolution is rarely upheld, with a more episodic view taking its place. This moves focus away from viewing phenotypic evolution as a simple homogeneous process and facilitates reconciliation with macroevolutionary interpretations from a genetic perspective, paving the way to novel insights into the link between genotype and phenotype. The ability to detect positive selection when genetic data are unavailable or unobtainable represents an attractive prospect for extant species, but when applied to fossil data it can reveal patterns of natural selection in deep time that would otherwise be impossible.

Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish

Background: Transgressive segregation describes the occurrence of novel phenotypes in hybrids with extreme trait values not observed in either parental species. A previously experimentally untested prediction is that the amount of transgression increases with the genetic distance between hybridizing species. This follows from QTL studies suggesting that transgression is most commonly due to complementary gene action or epistasis, which become more frequent at larger genetic distances. This is because the number of QTLs fixed for alleles with opposing signs in different species should increase with time since speciation provided that speciation is not driven by disruptive selection. We measured the amount of transgression occurring in hybrids of cichlid fish bred from species pairs with gradually increasing genetic distances and varying phenotypic similarity. Transgression in multi-trait shape phenotypes was quantified using landmark-based geometric morphometric methods. Results: We found that genetic distance explained 52% and 78% of the variation in transgression frequency in F1 and F2 hybrids, respectively. Confirming theoretical predictions, transgression when measured in F2 hybrids, increased linearly with genetic distance between hybridizing species. Phenotypic similarity of species on the other hand was not related to the amount of transgression. Conclusion: The commonness and ease with which novel phenotypes are produced in cichlid hybrids between unrelated species has important implications for the interaction of hybridization with adaptation and speciation. Hybridization may generate new genotypes with adaptive potential that did not reside as standing genetic variation in either parental population, potentially enhancing a population's responsiveness to selection. Our results make it conceivable that hybridization contributed to the rapid rates of phenotypic evolution in the large and rapid adaptive radiations of haplochromine cichlids.

Effects of Interspecific Gene Flow on the Phenotypic Variance-Covariance Matrix in Lake Victoria Cichlids

Quantitative genetics theory predicts adaptive evolution to be constrained along evolutionary lines of least resistance. In theory, hybridization and subsequent interspecific gene flow may however rapidly change the evolutionary constraints of a population and eventually change its evolutionary potential, but empirical evidence is still scarce. Using closely related species pairs of Lake Victoria cichlids sampled from four different islands with different levels of interspecific gene flow, we tested for potential effects of introgressive hybridization on phenotypic evolution in wild populations. We found that these effects differed among our study species. Constraints measured as the eccentricity of phenotypic variance-covariance matrices declined significantly with increasing gene flow in the less abundant species for matrices that have a diverged line of least resistance. In contrast we find no such decline for the more abundant species. Overall our results suggest that hybridization can change the underlying phenotypic variance-covariance matrix, potentially increasing the adaptive potential of such populations.

Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication

Advances in genome technology have facilitated a new understanding of the historical and genetic processes crucial to rapid phenotypic evolution under domestication(1,2). To understand the process of dog diversification better, we conducted an extensive genome-wide survey of more than 48,000 single nucleotide polymorphisms in dogs and their wild progenitor, the grey wolf. Here we show that dog breeds share a higher proportion of multi-locus haplotypes unique to grey wolves from the Middle East, indicating that they are a dominant source of genetic diversity for dogs rather than wolves from east Asia, as suggested by mitochondrial DNA sequence data(3). Furthermore, we find a surprising correspondence between genetic and phenotypic/functional breed groupings but there are exceptions that suggest phenotypic diversification depended in part on the repeated crossing of individuals with novel phenotypes. Our results show that Middle Eastern wolves were a critical source of genome diversity, although interbreeding with local wolf populations clearly occurred elsewhere in the early history of specific lineages. More recently, the evolution of modern dog breeds seems to have been an iterative process that drew on a limited genetic toolkit to create remarkable phenotypic diversity.

Parallel and nonparallel ecological, morphological and genetic divergence in lake-stream stickleback from a single catchment

Parallel phenotypic evolution in similar environments has been well studied in evolutionary biology; however, comparatively little is known about the influence of determinism and historical contingency on the nature, extent and generality of this divergence. Taking advantage of a novel system containing multiple lake-stream stickleback populations, we examined the extent of ecological, morphological and genetic divergence between three-spined stickleback present in parapatric environments. Consistent with other lake-stream studies, we found a shift towards a deeper body and shorter gill rakers in stream fish. Morphological shifts were concurrent with changes in diet, indicated by both stable isotope and stomach contents analysis. Performing a multivariate test for shared and unique components of evolutionary response to the distance gradient from the lake, we found a strong signature of parallel adaptation. Nonparallel divergence was also present, attributable mainly to differences between river locations. We additionally found evidence of genetic substructuring across five lake-stream transitions, indicating that some level of reproductive isolation occurs between populations in these habitats. Strong correlations between pairwise measures of morphological, ecological and genetic distance between lake and stream populations supports the hypothesis that divergent natural selection between habitats drives adaptive divergence and reproductive isolation. Lake-stream stickleback divergence in Lough Neagh provides evidence for the deterministic role of selection and supports the hypothesis that parallel selection in similar environments may initiate parallel speciation.

Epigenomic plasticity within populations: its evolutionary significance and potential

Epigenetics has progressed rapidly from an obscure quirk of heredity into a data-heavy ‘omic’ science. Our understanding of the molecular mechanisms of epigenomic regulation, and the extent of its importance in nature, are far from complete, but in spite of such drawbacks, population-level studies are extremely valuable: epigenomic regulation is involved in several processes central to evolutionary biology including phenotypic plasticity, evolvability and the mediation of intragenomic conflicts. The first studies of epigenomic variation within populations suggest high levels of phenotypically relevant variation, with the patterns of epigenetic regulation varying between individuals and genome regions as well as with environment. Epigenetic mechanisms appear to function primarily as genome defences, but result in the maintenance of plasticity together with a degree of buffering of developmental programmes; periodic breakdown of epigenetic buffering could potentially cause variation in rates of phenotypic evolution.