Understanding the factors influencing the current distribution of genetic diversity across a species range is one of the main questions of evolutionary biology, especially given the increasing threat to biodiversity posed by climate change. Historical demographic processes such as population expansion or bottlenecks and decline are known to exert a predominant influence on past and current levels of genetic diversity, and revealing this demo‐genetic history can have immediate conservation implications. We used a whole‐exome capture sequencing approach to analyze polymorphism across the gene space of red spruce (Picea rubens Sarg.), an endemic and emblematic tree species of eastern North America high‐elevation forests that are facing the combined threat of global warming and increasing human activities. We sampled a total of 340 individuals, including populations from the current core of the range in northeastern USA and southeastern Canada and from the southern portions of its range along the Appalachian Mountains, where populations occur as highly fragmented mountaintop “sky islands.” Exome capture baits were designed from the closely relative white spruce (P. glauca Voss) transcriptome, and sequencing successfully captured most regions on or near our target genes, resulting in the generation of a new and expansive genomic resource for studying standing genetic variation in red spruce applicable to its conservation. Our results, based on over 2 million exome‐derived variants, indicate that red spruce is structured into three distinct ancestry groups that occupy different geographic regions of its highly fragmented range. Moreover, these groups show small Ne , with a temporal history of sustained population decline that has been ongoing for thousands (or even hundreds of thousands) of years. These results demonstrate the broad potential of genomic studies for revealing details of the demographic history that can inform management and conservation efforts of nonmodel species with active restoration programs, such as red spruce.
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Genotypic variation and plasticity in climate-adaptive traits after range expansion and fragmentation of red spruce ( Picea rubens Sarg.)
Shifting range limits are predicted for many species as the climate warms. However, the rapid pace of climate change will challenge the natural dispersal capacity of long-lived, sessile organisms such as forest trees. Adaptive responses of populations will, therefore, depend on levels of genetic variation and plasticity for climate-responsive traits, which likely vary across the range due to expansion history and current patterns of selection. Here, we study levels of genetic and plastic variation for phenology and growth traits in populations of red spruce ( Picea rubens ), from the range core to the highly fragmented trailing edge. We measured more than 5000 offspring sampled from three genetically distinct regions (core, margin and edge) grown in three common gardens replicated along a latitudinal gradient. Genetic variation in phenology and growth showed low to moderate heritability and differentiation among regions, suggesting some potential to respond to selection. Phenology traits were highly plastic, but this plasticity was generally neutral or maladaptive in the effect on growth, revealing a potential liability under warmer climates. These results suggest future climate adaptation will depend on the regional availability of genetic variation in red spruce and provide a resource for the design and management of assisted gene flow. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’.
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- NSF-PAR ID:
- 10384035
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 377
- Issue:
- 1848
- ISSN:
- 0962-8436
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The rapid pace of contemporary environmental change puts many species at risk, especially rare species constrained by limited capacity to adapt or migrate due to low genetic diversity and/or fitness. But the ability to acclimate can provide another way to persist through change. We compared the capacity of rare
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Abstract Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungus
Batrachochytrium dendrobatidis (Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd. -
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The ability to respond to environmental changes plays a crucial role for coping with environmental stressors related to climate change. Substantial changes in environmental conditions can overcome developmental homeostasis, exposing cryptic genetic variation. The katydid
Neoconocephalus triops is a tropical species that extended its range to the more seasonal environment of North America where it has two reproductive generations per year. The harsher winter conditions required adults to diapause which resulted in substantially different mating calls of the diapausing winter animals compared to the non-overwintering summer animals in northern Florida. The summer call corresponds to that of tropical populations, whereas the winter call represents the alternative call phenotype. We quantified call plasticity in a tropical (Puerto Rico) and a temperate population ofN. triops (Florida) that differ in experiencing winter conditions in their geographic regions. We hypothesized that the plastic call traits, i.e., double-pulse rate and call structure, are regulated independently. Further, we hypothesized that phenotypic plasticity of double-pulse rate results in quantitative changes, whereas that of call structure in qualitative changes. We varied the photoperiod and duration of diapause during male juvenile and adult development during rearing and analyzed the double-pulse rate and call structure of the animals. Double-pulse rate changed in a quantitative fashion in both populations and significant changes appeared at different developmental points, i.e., the double-pulse rate slowed down during juvenile development in Florida, whereas during adult diapause in Puerto Rico. In the Florida population, both the number of males producing and the proportion of total call time covered by the alternative call structure (= continuous calls) increased with duration spent in diapause. In the Puerto Rico population, expression of the alternative call structure was extremely rare. Our results suggest that the expression of both pulse rate and call structure was quantitative and not categorical. Our systematic variation of environmental variables demonstrated a wide range of phenotypic variation that can be induced during development. Our study highlights the evolutionary potential of hidden genetic variation and phenotypic plasticity when confronted with rapidly changing environments and their potential role in providing variation necessary for communication systems to evolve. -
Synopsis Environmental variation experienced by a species across space and time can promote the maintenance of genetic diversity that may be adaptive in future global change conditions. Selection experiments have shown that purple sea urchin, Strongylocentrotus purpuratus, populations have adaptive genetic variation for surviving pH conditions at the “edge” (pH 7.5) of conditions experienced in nature. However, little is known about whether populations have genetic variation for surviving low-pH events beyond those currently experienced in nature or how variation in pH conditions affects organismal and genetic responses. Here, we quantified survival, growth, and allele frequency shifts in experimentally selected developing purple sea urchin larvae in static and variable conditions at three pH levels: pH 8.1 (control), pH 7.5 (edge-of-range), and pH 7.0 (extreme). Variable treatments recovered body size relative to static treatments, but resulted in higher mortality, suggesting a potential tradeoff between survival and growth under pH stress. However, within each pH level, allele frequency changes were overlapping between static and variable conditions, suggesting a shared genetic basis underlying survival to mean pH regardless of variability. In contrast, genetic responses to pH 7.5 (edge) versus pH 7.0 (extreme) conditions were distinct, indicating a unique genetic basis of survival. In addition, loci under selection were more likely to be in exonic regions than regulatory, indicating that selection targeted protein-coding variation. Loci under selection in variable pH 7.5 conditions, more similar to conditions periodically experienced in nature, performed functions related to lipid biosynthesis and metabolism, while loci under selection in static pH 7.0 conditions performed functions related to transmembrane and mitochondrial processes. While these results are promising in that purple sea urchin populations possess genetic variation for surviving extreme pH conditions not currently experienced in nature, they caution that increased acidification does not result in a linear response but elicits unique physiological stresses and survival mechanisms.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rstb.2021.0008
