An official website of the United States government
Intraspecific competition has long been considered a key driver of evolutionary diversification, but whether it can also promote evolutionary innovation is less clear. We examined the interplay between competition and phenotypic plasticity in fueling the origins of a novel, complex phenotype––a distinctive carnivore morph found in spadefoot toad tadpoles (genus Spea) that specializes on fairy shrimp. We specifically sought to explore the possible origins of this phenotype by providing shrimp to Scaphiopus holbrookii tadpoles (the sister genus to Spea that does not produce carnivores) while subjecting them to competition for their standard diet of detritus. Previous research had shown that this species will eat shrimp when detritus is limited, and that these shrimp-fed individuals produce features that are redolent of a rudimentary Spea carnivore. In this study, we found that: 1) behavioral and morphological plasticity enabled some individuals to expand their diet to include shrimp; 2) there was heritable variation in this plasticity; and 3) individuals received a growth and development benefit by eating shrimp. Thus, novel resource use can arise via plasticity as an adaptive response to intraspecific competition. More generally, our results show how competition and plasticity may interact to pave the way for the evolution of complex, novel phenotypes, such as the distinctive carnivore morph in present-day Spea.
more »
« less
Genetic accommodation in the wild: evolution of gene expression plasticity during character displacement
Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity (‘genetic accommodation’) mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separately in allopatry (the ancestral condition), each produces alternative, diet-induced, larval ecomorphs: omnivores, which eat detritus, and carnivores, which specialize on shrimp. By contrast, where these two species occur together in sympatry (the derived condition), selection to minimize competition for detritus has caused S. bombifrons to become nearly fixed for producing only carnivores, suggesting that character displacement might have arisen through an extreme form of genetic accommodation (‘genetic assimilation’) in which plasticity is lost. Here, we asked whether we could infer a signature of this process in regulatory changes of specific genes. In particular, we investigated whether genes that are normally expressed more highly in one morph (‘biased’ genes) have evolved reduced plasticity in expression levels among S. bombifrons from sympatry compared to S. bombifrons from allopatry. We reared individuals from sympatry vs. allopatry on detritus or shrimp and measured the reaction norms of nine biased genes. Although different genes displayed different patterns of gene regulatory evolution, the combined gene expression profiles revealed that sympatric individuals had indeed lost the diet-induced gene expression plasticity present in allopatric individuals. Our data therefore pro- vide one of the few examples from natural populations in which genetic accommodation/assimilation can be traced to regulatory changes of specific genes. Such genetic accommodation might mediate character displacement in many systems.
more »
« less
- Award ID(s):
- 1643239
- PAR ID:
- 10062446
- Date Published:
- Journal Name:
- Journal of evolutionary biology
- Volume:
- 30
- ISSN:
- 1010-061X
- Page Range / eLocation ID:
- 1712–1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Plasticity-first evolution (PFE) posits that novel features arise when selection refines pre-existing phenotypic plasticity into an adaptive phenotype. However, PFE is controversial because few tests have been conducted in natural populations. Here we present evidence that PFE fostered the origin of an evolutionary novelty that allowed certain amphibians to invade a new niche—a distinctive carnivore morph. We compared morphology, gene expression and growth of three species of spadefoot toad tadpoles when reared on alternative diets: Scaphiopus holbrookii, which (like most frogs) never produce carnivores; Spea multiplicata, which sometimes produce carnivores, but only through diet-induced plasticity; and Spea bombifrons, which often produce carnivores regardless of diet. Consistent with PFE, we found diet-induced plasticity—in morphology and gene expression—in Sc. holbrookii, adaptive refinement of this plasticity in Sp. multiplicata, and further refinement of the carnivore phenotype in Sp. bombifrons. Generally, phenotypic plasticity might play a significant, if underappreciated, role in evolutionary innovation.more » « less
-
Abstract Character displacement theory predicts that closely-related co-occurring species should diverge in relevant traits to reduce costly interspecific interactions such as competition or hybridization. While many studies document character shifts in sympatry, few provide corresponding evidence that these shifts are driven by the costs of co-occurrence. Black-capped (Poecile atricapillus) and mountain chickadees (Poecile gambeli) are closely-related, ecologically similar, and broadly distributed songbirds with both allopatric and sympatric populations. In sympatry, both species appear to suffer costs of their co-occurrence: (a) both species are in worse body condition compared to allopatry and (b) hybridization sometimes yields sterile offspring. Here, we explored character displacement in the songs of black-capped and mountain chickadees by characterizing variation in male songs from sympatric and allopatric populations. We found that mountain chickadees sing differently in sympatry versus allopatry. Specifically, they produced more notes per song, were more likely to include an extra introductory note, and produced a smaller glissando in their first notes compared to all other populations. Combined with previous research on social dominance and maladaptive hybridization between black-capped and mountain chickadees, we posit that differences in sympatric mountain chickadee song are population-wide shifts to reduce aggression from dominant black-capped chickadees and/or prevent maladaptive hybridization.more » « less
-
To obtain better insight into the mechanisms of selenium hyperaccumulation in Stanleya pinnata, transcriptome-wide differences in root and shoot gene expression levels were investigated in S. pinnata and related nonaccumulator Stanleya elata grown with or without 20 M selenate. Genes predicted to be involved in sulfate/selenate transport and assimilation or in oxidative stress resistance (glutathione-related genes and peroxidases) were among the most differentially expressed between species; many showed constitutively elevated expression in S. pinnata. A number of defense-related genes predicted to mediate synthesis and signaling of defense hormones jasmonic acid (JA, reported to induce sulfur assimilatory and glutathione biosynthesis genes), salicylic acid (SA) and ethylene were also more expressed in S. pinnata than S. elata. Several upstream signaling genes that upregulate defense hormone synthesis showed higher expression in S. pinnata than S. elata and might trigger these selenium-mediated defense responses. Thus, selenium hyperaccumulation and hypertolerance in S. pinnata may be mediated by constitutively upregulated JA, SA and ethylene-mediated defense systems, associated with elevated expression of genes involved in sulfate/selenate uptake and assimilation or in antioxidant activity. Genes pinpointed in this study may be targets of genetic engineering of plants that may be employed in biofortification or phytoremediation.more » « less
-
Wittkopp, Patricia (Ed.)Abstract Cytonuclear coordination between biparental-nuclear genomes and uniparental-cytoplasmic organellar genomes in plants is often resolved by genetic and transcriptional cytonuclear responses. Whether this mechanism also acts in allopolyploid members of other kingdoms is not clear. Additionally, cytonuclear coordination of interleaved allopolyploid cells/individuals within the same population is underexplored. The yeast Saccharomyces pastorianus provides the opportunity to explore cytonuclear coevolution during different growth stages and from novel dimensions. Using S. pastorianus cells from multiple growth stages in the same environment, we show that nuclear mitochondria-targeted genes have undergone both asymmetric gene conversion and growth stage-specific biased expression favoring genes from the mitochondrial genome donor (Saccharomyces eubayanus). Our results suggest that cytonuclear coordination in allopolyploid lager yeast species entails an orchestrated and compensatory genetic and transcriptional evolutionary regulatory shift. The common as well as unique properties of cytonuclear coordination underlying allopolyploidy between unicellular yeasts and higher plants offers novel insights into mechanisms of cytonuclear evolution associated with allopolyploid speciation.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/doi: 10.1111/jeb.13133
