More Like this

1. Adaptive radiation despite conserved modularity patterns in San Salvador Island Cyprinodon pupfishes and their hybrids

   https://doi.org/10.1093/evolinnean/kzae013  

   Chan, HoWan; Colaco, Emma; Martin, Christopher H; Evans, Kory M (January 2024, Evolutionary Journal of the Linnean Society)

   Abstract Adaptive radiations are striking examples of rapid speciation along ecological lines. In adaptive radiations, fast rates of lineage diversification often pair with rapid rates of morphological diversification. Such diversification has often been documented through the lens of ecological drivers, overlooking the intrinsic structural constraints that may also have a key role in configuring patterns of trait diversification. Covariation within and between traits has been hypothesized to govern the axes of trait evolution, either by increasing the degree of covariation between traits (i.e. integration), which promotes morphological coordination, or by strengthening the degree of covariation within traits (i.e. modularity), which allows organisms to explore novel trait combinations and different regions of morphospace. Here, we study the modularity of the skull within an adaptive radiation of pupfishes that is endemic to San Salvador Island, Bahamas. This radiation exhibits divergent craniofacial morphologies, including generalist, snail-eating specialist, and scale-eating specialist species. We assessed morphological disparity, integration strength, and modularity patterns across the sympatric San Salvador Island pupfish radiation, lab-reared hybrids, and closely related outgroup species. Our findings revealed an unexpected uniformity in the pattern of modularity across diverse species, supporting a five-module functional hypothesis comprising the oral jaw, pharyngeal jaw, neurocranium, hyoid apparatus, and hyomandibula. Despite this conserved modularity pattern, all species exhibited weak but significantly varying strengths of overall between-module integration and significant disparity across all cranial regions. Our results suggest rapid morphological diversification can occur even with conserved patterns of modularity. We propose that broadscale patterns of modularity are more conserved while between-module associations are more evolvable between species. 

   more » « less
2. We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

   https://doi.org/10.1098/rspb.2022.0613  

   Richards, Emilie J.; Martin, Christopher H. (May 2022, Proceedings of the Royal Society B: Biological Sciences)

   Adaptive radiations involve astounding bursts of phenotypic, ecological and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of an intermediate C. sp. ‘wide-mouth’ scale-eating ecomorph in a sympatric radiation of Cyprinodon pupfishes, illuminating the transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct and often consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in trophic specialists to characterize their adaptive walk. Shared adaptive regions swept first in both the specialist desquamator and the intermediate ‘wide-mouth’ ecomorph, followed by unique sweeps of introgressed variation in ‘wide-mouth’ and de novo variation in desquamator . The two scale-eating populations additionally shared 9% of their hard selective sweeps with the molluscivore C. brontotheroides , despite no single common ancestor among specialists. Our work provides a new microevolutionary framework for investigating how major ecological transitions occur and illustrates how both shared and unique genetic variation can provide a bridge for multiple species to access novel ecological niches. 

   more » « less
3. PRJNA833158 Characterizing a new 'wide-mouth' scale-eating ecomorph in San Salvador Island Cyprinodon pupfish radiation

   Richards, EJ; Martin, CH (April 2022, NCBI)

   Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of an intermediate wide-mouth scale-eating ecomorph in a sympatric radiation of Cyprinodon pupfishes, illuminating the transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct, and often consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in trophic specialists to characterize their adaptive walk. Shared adaptive regions swept first in both the specialist desquamator and the intermediate wide-mouth ecomorph, followed by unique sweeps of introgressed variation in wide-mouth and de novo variation in desquamator. The two scale-eating populations additionally shared 9% of their hard selective sweeps with molluscivores C. brontotheroides, despite no single common ancestor among specialists. Our work provides a new microevolutionary framework for investigating how major ecological transitions occur and illustrates how both shared and unique genetic variation can provide a bridge for multiple species to access novel ecological niches. 

   more » « less
4. Few Fixed Variants between Trophic Specialist Pupfish Species Reveal Candidate Cis -Regulatory Alleles Underlying Rapid Craniofacial Divergence

   https://doi.org/10.1093/molbev/msaa218  

   McGirr, Joseph A; Martin, Christopher H (September 2020, Molecular Biology and Evolution)

   Wittkopp, Patricia (Ed.)

   Abstract Investigating closely related species that rapidly evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying variation in complex traits. This can also lead to the discovery of novel candidate genes influencing natural and clinical variation in human craniofacial phenotypes. We combined whole-genome resequencing of 258 individuals with 50 transcriptomes to identify candidate cis-acting genetic variation underlying rapidly evolving craniofacial phenotypes within an adaptive radiation of Cyprinodon pupfishes. This radiation consists of a dietary generalist species and two derived trophic niche specialists—a molluscivore and a scale-eating species. Despite extensive morphological divergence, these species only diverged 10 kya and produce fertile hybrids in the laboratory. Out of 9.3 million genome-wide SNPs and 80,012 structural variants, we found very few alleles fixed between species—only 157 SNPs and 87 deletions. Comparing gene expression across 38 purebred F1 offspring sampled at three early developmental stages, we identified 17 fixed variants within 10 kb of 12 genes that were highly differentially expressed between species. By measuring allele-specific expression in F1 hybrids from multiple crosses, we found that the majority of expression divergence between species was explained by trans-regulatory mechanisms. We also found strong evidence for two cis-regulatory alleles affecting expression divergence of two genes with putative effects on skeletal development (dync2li1 and pycr3). These results suggest that SNPs and structural variants contribute to the evolution of novel traits and highlight the utility of the San Salvador Island pupfish system as an evolutionary model for craniofacial development. 

   more » « less
5. Adaptive Radiation Genomics of Two Ecologically Divergent Hawai‘ian Honeycreepers: The ‘akiapōlā‘au and the Hawai‘i ‘amakihi

   https://doi.org/10.1093/jhered/esz057  

   Campana, Michael G; Corvelo, André; Shelton, Jennifer; Callicrate, Taylor E; Bunting, Karen L; Riley-Gillis, Bridget; Wos, Frank; DeGrazia, Justin; Jarvis, Erich D; Fleischer, Robert C (November 2019, Journal of Heredity)

   Gillespie, Rosemary (Ed.)

   Abstract The Hawai‘ian honeycreepers (drepanids) are a classic example of adaptive radiation: they adapted to a variety of novel dietary niches, evolving a wide range of bill morphologies. Here we investigated genomic diversity, demographic history, and genes involved in bill morphology phenotypes in 2 honeycreepers: the ‘akiapōlā‘au (Hemignathus wilsoni) and the Hawai‘i ‘amakihi (Chlorodrepanis virens). The ‘akiapōlā‘au is an endangered island endemic, filling the “woodpecker” niche by using a unique bill morphology, while the Hawai‘i ‘amakihi is a dietary generalist common on the islands of Hawai‘i and Maui. We de novo sequenced the ‘akiapōlā‘au genome and compared it to the previously sequenced ‘amakihi genome. The ‘akiapōlā‘au is far less heterozygous and has a smaller effective population size than the ‘amakihi, which matches expectations due to its smaller census population and restricted ecological niche. Our investigation revealed genomic islands of divergence, which may be involved in the honeycreeper radiation. Within these islands of divergence, we identified candidate genes (including DLK1, FOXB1, KIF6, MAML3, PHF20, RBP1, and TIMM17A) that may play a role in honeycreeper adaptations. The gene DLK1, previously shown to influence Darwin’s finch bill size, may be related to honeycreeper bill morphology evolution, while the functions of the other candidates remain unknown. 

   more » « less