Eco-evolutionary processes underlying species range shifts are fundamental to understand the distribution of organisms. Interest in such processes, particularly those associated with range expansion, has increased because of unprecedented rates of climate change. Recent theoretical work suggests intrinsic factors, i.e., demographic dynamics, during expansions may lead to reduced genetic diversity and the accumulation of deleterious alleles (expansion load), decreasing the species ability to adapt and thus limiting its expansion and distribution. Yet, empirical field studies testing these predictions in natural settings remain rather scarce and show contrasting results. In this thesis, we use the short-lived colonizing plant Leontodon longirostris to produce new empirical evidence of the evolutionary dynamics and consequences of range expansion in the Iberian Peninsula along a climatic gradient. To that end, we first produced a first genome draft for the species, covering c.a. 50% of the genome, and we use it to sequence 238 individuals from 21 populations in the Iberian Peninsula to infer the demographic history of the species and the patterns of genetic diversity and load associated to the expansion process. Second, to obtain phenotypic evidence for adaptation, we assess the variability in 42 populations for key life history traits related to the timing of germination, flowering, and senescence. Finally, we use the same set of sequences described above, to search for genomic signatures of selection, to relate phenotypic and genetic variation, and to determine the relative contribution of standing and novel genetic variation to adaptation. Our results from the different demographic scenarios tested indicate that the overall demographic history was a northward expansion that, as expected, was accompanied by a loss of genetic diversity and an increase in expansion load. The patterns of phenotypic variability strongly suggest an adaptive cline for most life-history transitions. We find a continuous range of germination behavior and lifecycle variability, from annuality to iteroparity, following a gradient of decreasing aridity. Genotypes from drier habitats show overall lower germination rates and more restricted conditions for germination. Seedlings from warmer and drier habitats emerge later and flower earlier. Consequently, plants from the southern localities, growing in more unpredictable and stressful arid environments, show a shorter lifespan, attain smaller sizes at reproduction, but also allocate more biomass to reproduction. Support for the range-wide role of selective processes leading to adaptation is also provided by genomic analyses. The comparison of selective sweeps between core and range-front populations provides further evidence that adaptation to both novel biotic and abiotic conditions occurred during the northward expansion. The significant increase in the proportion of putative soft sweeps in front populations compared to those in the core range suggests that standing variation has played a prominent role for rapid adaptation to the novel environmental challenges associated with migration into northern habitats. We identify several candidate genes (among them, ACS7, MTN2, PHYE and NRT2.7) mainly acting in signaling pathways related to germination and flowering, and potentially mediating the phenological changes detected at the phenotypic level. Summer precipitation and minimum temperatures of winter and spring seem to be the key environmental cues driving the variation found in genes putatively involved in germination and flowering, respectively. Overall, then, and contrary to some theoretical expectations and empirical data, in this study system the genetic load accumulated during demographic expansion does not seem to prevent the species and its populations to adapt to novel selection pressures. Adaptation in spite genetic load was probably possible due to other eco-evolutionary processes involving some other important traits, among them the high dispersal capacity and the self-incompatible mating system of the species.
|Date of Award||19 Apr 2021|
|Supervisor||Miquel Riba Rovira (Tutor) & Maria Mayol Martínez (Director)|