Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of “trait remixing” in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.
This content will become publicly available on June 9, 2024
- Award ID(s):
- 2151540
- NSF-PAR ID:
- 10429118
- Date Published:
- Journal Name:
- Biological Journal of the Linnean Society
- Volume:
- 139
- Issue:
- 3
- ISSN:
- 0024-4066
- Page Range / eLocation ID:
- 243 to 256
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract Understanding the processes that drive divergence within and among species is a long‐standing goal in evolutionary biology. Traditional approaches to assessing differentiation rely on phenotypes to identify intra‐ and interspecific variation, but many species express subtle morphological gradients in which boundaries among forms are unclear. This intraspecific variation may be driven by differential adaptation to local conditions and may thereby reflect the evolutionary potential within a species. Here, we combine genetic and morphological data to evaluate intraspecific variation within the Nelson's (
Ammodramus nelsoni ) and salt marsh (Ammodramus caudacutus ) sparrow complex, a group with populations that span considerable geographic distributions and a habitat gradient. We evaluated genetic structure among and within five putative subspecies ofA. nelsoni andA. caudacutus using a reduced‐representation sequencing approach to generate a panel of 1929SNP s among 69 individuals. Although we detected morphological differences among some groups, individuals sorted along a continuous phenotypic gradient. In contrast, the genetic data identified three distinct clusters corresponding to populations that inhabit coastal salt marsh, interior freshwater marsh and coastal brackish–water marsh habitats. These patterns support the current species‐level recognition but do not match the subspecies‐level taxonomy within each species—a finding which may have important conservation implications. We identified loci exhibiting patterns of elevated divergence among and within these species, indicating a role for local selective pressures in driving patterns of differentiation across the complex. We conclude that this evidence for adaptive variation among subspecies warrants the consideration of evolutionary potential and genetic novelty when identifying conservation units for this group. -
more » « less
Abstract Sexual signalling traits are often observed to diverge rapidly among populations, thereby playing a potentially key early role in the evolution of reproductive isolation. While often assumed to reflect divergent sexual selection among populations, patterns of sexual trait diversification might sometimes be biased along axes of standing additive genetic variation and covariation among trait components. Additionally, theory predicts that environmentally induced phenotypic variation might facilitate rapid trait evolution, suggesting that patterns of divergence between populations should mirror phenotypic plasticity within populations. Here, we evaluate the concordance between observed axes of multivariate sexual trait divergence and predicted divergence based on (1) interpopulation variation in sexual selection, (2) additive genetic variances and (3) temperature‐related phenotypic plasticity in male courtship song among geographically isolated populations of the Hawaiian swordtail cricket,
Laupala cerasina , which exhibit sexual isolation due acoustic signalling traits. The major axis of multivariate divergence,d max, accounted for 76% of variation among population male song trait means and was moderately correlated with interpopulation differences in directional sexual selection based on female preferences. However, the majority of additive genetic variance was largely oriented away from the direction of divergence, suggesting that standing genetic variation may not play a dominant role in the patterning of signal divergence. In contrast, the axis of phenotypic plasticity strongly mirrored patterns of interpopulation phenotypic divergence, which is consistent with a role for temperature‐related plasticity in facilitating instead of inhibiting male song evolution and sexual isolation in these incipient species. We propose potential mechanisms by which sexual selection might interact with phenotypic plasticity to facilitate the rapid acoustic diversification observed in this species and clade. -
more » « less
Abstract Phenotypic differentiation in size and fecundity between native and invasive populations of a species has been suggested as a causal driver of invasion in plants. Local adaptation to novel environmental conditions through a micro‐evolutionary response to natural selection may lead to phenotypic differentiation and fitness advantages in the invaded range. Local adaptation may occur along a stress tolerance trade‐off, favoring individuals that, in benign conditions, shift resource allocation from stress tolerance to increased vigor and fecundity and, therefore, invasiveness. Alternately, the typically disturbed invaded range may select for a plastic, generalist strategy, making phenotypic plasticity the main driver of invasion success. To distinguish between these hypotheses, we performed a field common garden and tested for genetically based phenotypic differentiation, resource allocation shifts in response to water limitation, and local adaptation to the environmental gradient which describes the source locations for native and invasive populations of diffuse knapweed (
C entaurea diffusa)C. diffusa populations produced larger, later maturing, and therefore potentially fitter individuals than native populations. Evidence for local adaptation along a resource allocation trade‐off for water limitation tolerance is equivocal. However, native populations do show evidence of local adaptation to an environmental gradient, a relationship which is typically not observed in the invaded range. Broader analysis of the climatic niche inhabited by the species in both ranges suggests that the physiological tolerances ofC. diffusa may have expanded in the invaded range. This observation could be due to selection for plastic, “general‐purpose” genotypes with broad environmental tolerances. -
more » « less
Abstract Long‐term environmental variation often drives local adaptation and leads to trait differentiation across populations. Additionally, when traits change in an environment‐dependent way through phenotypic plasticity, the genetic variation underlying plasticity will also be under selection. These processes could create a landscape of differentiation across populations in traits and their plasticity. Here, we performed a dry‐down experiment under controlled conditions to measure responses in seedlings of a shrub species from the Cape Floristic Region, the common sugarbush (
Protea repens ). We measured morphological and physiological traits, and sequenced whole transcriptomes of leaf tissues from eight populations that represent both the climatic and the geographical distribution of this species. We found that there is substantial variation in how populations respond to drought, but we also observed common patterns such as reduced leaf size and leaf thickness, and up‐regulation of stress‐related and down‐regulation of growth‐related gene groups. Both high environmental heterogeneity and milder source site climates were associated with higher plasticity in various traits and co‐expression gene networks. Associations between traits, trait plasticity, gene networks and the source site climate suggest that temperature may play a greater role in shaping these patterns when compared to precipitation, in line with recent changes in the region due to climate change. We also found that traits respond to climatic variation in an environment‐dependent manner: some associations between traits and climate were apparent only under certain growing conditions. Together, our results uncover common responses ofP. repens populations to drought, and climatic drivers of population differentiation in functional traits, gene expression and their plasticity.
