Biology subjects

Martin, C. H.

Publications and source records attributed to Martin, C. H..

At least 19 recordsLinked to original sources

bioRxiv2026

Rescued from extinction in two buckets: genomic consequences of an extreme bottleneck in the endangered Owens pupfish

Rapid population bottlenecks can threaten population viability by reducing genetic diversity and effective population size while increasing inbreeding. Freshwater fishes are particularly vulnerable to bottlenecks due to habitat fragmentation, water extraction, and invasive species. The Owens pupfish (Cyprinodon radiosus) is an endangered freshwater fish endemic to Owens Valley, CA that was originally thought to be extinct prior to rediscovery in 1964. In 1969, Edwin (Phil) Pister famously saved the entire species from extinction in two buckets after learning that the sole spring they inhabited was drying up. Today, six extant refuge populations ranging in size from 100 - 10,000 individuals remain, which all descend from this severe bottleneck of an estimated 400 individuals. Here, we sequenced whole genomes of 12 individuals from two populations (one extirpated, one extant) to reconstruct recent demographic history and examine the genomic consequences of this well-documented bottleneck on genetic diversity, effective population size, and inbreeding in the Owens pupfish. We estimated the timing of the bottleneck precisely to 1977-1985, closely coinciding with its documented history. Genetic diversity is low across the genome and the bottleneck caused a 17-fold contraction in effective population size over the span of 8 generations. We found low levels of inbreeding that likely predated the bottleneck. Our results suggest that Owens pupfish are threatened by reduced genetic diversity and low effective population size which may constrain adaptive potential, but that recent inbreeding is unlikely to be a serious concern due to population expansion. Our study highlights how the long-term effects of bottlenecks depend not only on severity, but also duration and the rate of population growth afterwards.

evolutionary biology↗

bioRxiv2026

Rapid divergence in sperm morphology and transgressive segregation of hybrid sperm kinematics in a young pupfish radiation

Understanding how divergence in reproductive traits can promote speciation remains a fundamental question in evolutionary biology. Sperm morphology and kinematics diverge rapidly across species. However, the effect of hybridization between recently diverged species on sperm traits remains unclear, limiting our understanding of how reproductive isolation evolves. Here, we evaluated sperm morphology, kinematics, and trait integration in species of a young (~10,000 years), sympatric Cyprinodon pupfish radiation from San Salvador Island, Bahamas, as well as fertile advanced-generation hybrids between two of these species. We found significant divergence in flagellum length, midpiece area, and sperm velocity among species. In contrast, hybrids displayed transgressive kinematic profiles defined by high velocities, reduced path curvature, and distinct patterns of sperm kinematic integration. Our findings suggest that hybridization between recently diverged species may reorganize the underlying control of sperm locomotor mechanisms, generating novel phenotypes that could contribute to reproductive isolation in the early stages of speciation.

evolutionary biology↗

bioRxiv2026

Long-term small effective population size, inbreeding, and a recessive lethal haplotype drive premature death in the endangered Devils Hole pupfish (Cyprinodon diabolis)

As anthropogenic habitat fragmentation and population decline accelerate globally, growing numbers of species face compounding demographic and genetic threats to long-term survival. Many populations are already forced to persist at chronically small sizes, yet the genomic and fitness consequences of this fate remain poorly understood. Here we leverage the demographic history of the Devils Hole pupfish to investigate how long-term small population size and recent bottlenecks have shaped genetic diversity, genetic load, inbreeding, and fitness through comparative population genomics, historical sequencing, and sampling embryos that died prematurely during development. We find that genetic diversity in Devils Hole pupfish is among the lowest recorded in the wild and that fixed load is high, consistent with thousands of generations of isolation at small population size. Even in the face of this low diversity and high fixed load, we show that inbreeding is still strongly associated with premature embryonic death, which affects up to 25% of offspring in the captive refuge and can be identified in advance based on a characteristic elongated heart tube and reduced heart rate. We discovered a recessive lethal haplotype segregating at [~]20% frequency that accounts for 50% of embryonic deaths and contains mutations in MIB1 and MMP16, genes associated with cardiomyopathy and atrial fibrillation. Our findings link genotype, phenotype, and fitness in an iconic endangered species to provide a rare comprehensive view into the evolutionary dynamics and consequences of long-term small effective population size, demonstrating that endangered species remain vulnerable to inbreeding depression despite extremely low genetic diversity.

evolutionary biology↗

bioRxiv2026

Global adaptation to climate change in the twilight zone revealed by shared signals of selection in mesopelagic lanternfishes

Rapid accumulation of greenhouse gases threatens humanity and global diversity. The oceans absorb 30% of anthropogenic carbon emissions annually, but adaptation to climate change by the biotic components of this sink are poorly understood. Lanternfishes (Myctophiformes) are the most abundant vertebrates on the planet by biomass and the dominant mesopelagic vertebrate consumers, thus crucial components of the global carbon cycle. However, it is unknown whether lanternfishes are adapting to global warming and ocean acidification (OA). We hypothesized that warming and OA would act as major shared selective forces across diverse oceanic environments and that disparate taxa would respond in parallel through shared genetic pathways. We used whole-genome sequencing to test this hypothesis by identifying shared signals of selection across lanternfishes from multiple sites in the Atlantic and Pacific spanning three genera (Benthosema glaciale, Triphoturus mexicanus, and Diaphus theta). Across all species we found evidence of expansion from a population bottleneck possibly corresponding to the last glacial maximum and effective population sizes of only 5 million, suggesting substantial reproductive skew and spatially restricted populations. We successfully identified 34 candidate genes experiencing strong shared selection pressure across all taxa in both oceans. 81% of these candidate genes were consistent with adaptations to warming and OA, including a heat-shock protein (HSP70) and genes related to skeletal development, calcium homeostasis, and biomineralization. 14 out of 34 candidate genes are also known from experimental climate change studies to be involved in the response to hypoxia, altered pH, and thermal stress. We found significant gene ontology enrichment within these candidates for otolith morphogenesis, a major component of OA adaptation in fishes. This study provides a new approach for studying climate change adaptation at a global scale and our results imply widespread shared adaptive responses of marine species to climate change.

evolutionary biology↗

bioRxiv2026

Estimate of the mutation rate in the endangered Devils Hole pupfish provides support for the drift-barrier hypothesis at an outlying extreme

Mutation rates vary by orders of magnitude across eukaryotes. The drift-barrier hypothesis proposes that drift overwhelms selection for lower mutation rates in small populations, leading to higher mutation rates over time due to the gradual accumulation of mutator alleles. Here, we test this hypothesis in one of the smallest long-term isolated populations in the world, the endangered Devils Hole pupfish (Cyprinodon diabolis). We estimated germline mutation rates in adults and embryos that died prematurely using autozygous segments due to recent inbreeding events. Our estimate of 8.09 x 10-9 per base pair per generation was higher than the mean rate for actinopterygian fishes of 5.97 x 10-9 (95% CI: 4.39 x 10-9 - 7.55 x 10-9) but was lower than predicted for such a low effective population size based on a recent meta-analysis of vertebrate mutation rates and similar to species with much larger effective population sizes, contradicting the drift barrier hypothesis. We also found that embryos which died during development had a higher mutation rate than mature adults, potentially reflecting a segregating lethal mutator allele. We analyzed the mutational spectra of germline mutations and found that spectra between embryonic lethal and mature adults were similar and comparable to other fishes, despite environmental differences in temperature, oxygen saturation, and UV exposure. Mutation rates in this endangered species provide new insights into the mechanisms driving mutation rate variation across vertebrates at one extreme of low effective population size in nature.

evolutionary biology↗

bioRxiv2025

Parallel and non-parallel features of adaptive radiation in Yucatan pupfishes

Understanding the extent of parallelism across adaptive radiations remains a central problem in evolutionary biology. We used whole-genome resequencing of 123 individuals to compare the adaptive radiation of Cyprinodon pupfishes in Lake Chichancanab, Mexico, to an independent radiation of San Salvador Island (SSI) pupfishes in the Bahamas, and assess the repeatability of adaptive genetic architecture, sources of adaptive variation, and stages of selection. Despite rapid craniofacial divergence of trophic specialists within 8-15 kya, only two candidate genes (0.5%; 2/426) were shared between Caribbean radiations. Although adaptive introgression played a major role in SSI, we found minimal evidence of adaptive introgression in Chichancanab, likely due to the geographic isolation of this inland lake. Instead, de novo mutations provided a substantial source of adaptive variation (30.6%) for the endemic zooplanktivore, 15 times higher than the endemic scale-eater on SSI. However, in parallel with SSI, we found strong evidence that adaptive divergence occurred in stages, first on regulatory and standing genetic variation, then on de novo and nonsynonymous mutations. Consistent with adaptive variants near opsin and spermatogenesis genes, functional categories unique to Chichancanab, we found greater visual acuity and divergent sperm morphology in lab-reared zooplanktivores relative to generalists using laboratory assays. Consistent with extensive adaptive de novo mutations in WNT10A and rapid diversification of tooth size in the zooplanktivore, we found that experimental inhibition of the Wnt pathway in generalists resulted in narrower oral teeth. We conclude that de novo mutations, not introgression, can drive rapid adaptive radiations in isolated environments.

evolutionary biology↗

bioRxiv2025

Adaptive radiation along ecological and morphological lines of least resistance in Cyprinodon pupfishes

Adaptive radiation results in part from ecological opportunity in a new environment, but it is unclear how pre-existing constraints in the founding population may limit this process. Genetic lines of least resistance, and by proxy morphological variance, are known to limit adaptive divergence, but ecological variance is rarely investigated. Here we test whether ecological or morphological lines of least resistance in generalist populations may have constrained the directions of species divergence in two independent Caribbean adaptive radiations of Cyprinodon pupfishes. We find almost universal congruence between the major multivariate dimensions of intraspecific craniofacial and dietary variance within generalist populations and the major axes of interspecific divergence within each adaptive radiation. This is surprising given that we document unique trophic specialists within each radiation, including a bivalve-specialist, zooplanktivore, molluscivore/ostracod-specialist, and scale-eating specialist, while nearly all generalist populations were observed to feed rarely on these same resources. We conclude that pre-existing genetic constraints within each founding generalist population, resulting in dimensions of greater ecological and morphological variance, may partially constrain and predict the directions of species divergence and dietary specialization during adaptive radiation. We also provide a new framework for examining ecological lines of least resistance.

evolutionary biology↗

bioRxiv2024

Tissue-specific transcriptomics uncovers novel craniofacial genes underlying jaw divergence in specialist pupfishes

The regulation of gene expression is one of the key evolutionary processes driving phenotypic divergence among species. Here, we investigate the tissue-specific gene expression of a non-model adaptive radiation of Cyprinodon pupfishes, characterized by their divergent dietary niches and exceptionally fast rates of craniofacial evolution. By comparing tissue-specific gene expression in the most morphologically divergent skeletal structure, the oral jaws, with the relatively morphologically conserved caudal tail region, we identified genes that were differentially expressed exclusively in the developing jaws of each of the three trophic specialists at hatching (8 dpf) and not in any other species. We then assessed their overlap (as transcriptionally-regulated genes) with adaptive regulatory variants identified in previous genomic studies. Our analysis identified pycr3 and atp8a1 as the most promising for craniofacial evolution in the scale-eaters, both genes with no known previous craniofacial function. We functionally confirmed the craniofacial expression of these genes by in situ mRNA hybridization chain reaction and demonstrated their species-specific expression in branchial and muscle tissues between sister species of this young radiation. Our work underscores the power of integrating tissue-specific transcriptomics with speciation genomics to identify novel craniofacial candidate genes controlling divergent morphogenesis in a natural evolutionary mutant system.

developmental biology↗

bioRxiv2024

The West African lungfish secretes a living cocoon during aestivation with uncertain antimicrobial function

One of the most exceptional adaptations to extreme drought is found in the sister group to tetrapods, the lungfishes (Dipnoi), which can aestivate inside a mucus cocoon for multiple years at reduced metabolic rates with complete cessation of ingestion and excretion. However, the function of the cocoon tissue is not fully understood. Here we developed a new more natural laboratory protocol for inducing aestivation in the West African lungfish, Protopterus annectens, and investigated the structure and function of the cocoon. We used electron microscopy and imaging of live tissue-stains to confirm that the inner and outer layers of the paper-thin cocoon are composed primarily of living cells. However, we also repeatedly observed extensive bacterial and fungal growth covering the cocoon and found no evidence of anti-microbial activity in vitro against E. coli for the cocoon tissue in this species. This classroom discovery-based research, performed during a course-based undergraduate research experience course (CURE), provides a robust laboratory protocol for investigating aestivation and calls into the question the function of this bizarre vertebrate adaptation.

physiology↗

bioRxiv2023

Discovery of a new craniofacial gene influencing adaptive phenotypes in a non-model pupfish radiation

Understanding the genetic basis of novel adaptations in new species is a fundamental question in biology that also provides an opportunity to uncover new genes and regulatory networks with potential clinical relevance. Here we demonstrate a new role for galr2 in vertebrate craniofacial development using an adaptive radiation of trophic specialist pupfishes endemic to San Salvador Island in the Bahamas. We confirmed the loss of a putative Sry transcription factor binding site in the upstream region of galr2 in scale-eating pupfish and found significant spatial differences in galr2 expression among pupfish species in Meckels cartilage and premaxilla using in situ hybridization chain reaction (HCR). We then experimentally demonstrated a novel function for Galr2 in craniofacial development and jaw elongation by exposing embryos to drugs that inhibit Galr2 activity. Galr2-inhibition reduced Meckels cartilage length and increased chondrocyte density in both trophic specialists but not in the generalist genetic background. We propose a mechanism for jaw elongation in scale-eaters based on the reduced expression of galr2 due to the loss of a putative Sry binding site. Fewer Galr2 receptors in the scale-eater Meckels cartilage may result in their enlarged jaw lengths as adults by limiting opportunities for a postulated Galr2 agonist to bind to these receptors during development. Our findings illustrate the growing utility of linking candidate adaptive SNPs in non-model systems with highly divergent phenotypes to novel vertebrate gene functions.

developmental biology↗

bioRxiv2021

Severe inbreeding and gene loss in the historical and extant population of the critically endangered Devils Hole pupfish

Small populations with limited geographic distributions are predicted to be threatened by inbreeding and lack of genetic diversity, both of which may negatively impact fitness and exacerbate population decline. One of the most extreme natural examples is the Devils Hole pupfish (Cyprinodon diabolis), an iconic and critically endangered species with the smallest known habitat range of any vertebrate. This imperiled species has experienced severe declines in population size over the last thirty years and suffered major, repeated bottlenecks in 2007 and 2013, when the population sunk to 38 and 35 individuals, respectively. Here we sequenced contemporary and historical genomes of Devils Hole and neighboring Death Valley and Ash Meadows desert pupfishes to examine the genomic consequences of small population size. We found extreme inbreeding (FROH = 0.71 - 0.82) and increased genetic load in the Devils Hole pupfish. We also document unique fixed loss-of-function (LOF) alleles and deletions in genes associated with sperm motility, stress, and hypoxia within the extant Devils Hole pupfish population that likely reduce fitness. Comparisons between contemporary samples (2008 - 2012) and a genome sequenced from a 1980 formalin-fixed museum specimen suggest that inbreeding has increased 6% as the population has declined, but that many putatively deleterious variants have been segregating in the population since at least 1980. This includes a fixed early stop codon in cfap43 (n = 8/8 samples), which is associated with sperm flagellum defects and causes infertility in humans and mice. Out of ninety-four unique deletions, fifteen were detected within 2 kb of annotated genes. Five have roles in physiological responses to hypoxia and mitochondrial activity, such as redd1 (n = 7/7 samples), suggesting impaired hypoxia tolerance in this species despite the low oxygen concentrations of Devils Hole. We thus document one of the most extreme inbreeding events in a natural population and a set of candidate deleterious variants to inform management and potential genetic rescue in this conservation icon.

evolutionary biology↗

bioRxiv2021

Diversity begets diversity through shared adaptive genetic variation: discovery of a cryptic wide-mouthed scale-eater

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.

evolutionary biology↗

bioRxiv2021

Parallel genetic changes underlie integrated craniofacial traits in an adaptive radiation of trophic specialist pupfishes

Many factors such as divergence time, shared standing genetic variation, frequency of introgression, and mutation rates can influence the likelihood of whether populations adapt to similar environments via parallel or non-parallel genetic changes. However, the frequency of parallel vs non-parallel genetic changes resulting in parallel phenotypic evolution is still unknown. In this study, we used a QTL mapping approach to investigate the genetic basis of highly divergent craniofacial traits between scale- and snail-eating trophic specialist species across similar hypersaline lake environments in an adaptive radiation of pupfishes endemic to San Salvador Island, Bahamas. We raised F2 intercrosses of scale- and snail-eaters from two different lake populations of sympatric specialists, estimated linkage maps, scanned for significant QTL for 30 skeletal and craniofacial traits, and compared the location of QTL between lakes to quantify parallel and non-parallel genetic changes. We found strong support for parallel genetic changes in both lakes for five traits in which we detected a significant QTL in at least one lake. However, many of these shared QTL affected different, but highly correlated craniofacial traits in each lake, suggesting that pleiotropy and trait integration should not be neglected when estimating rates of parallel evolution. We further observed a 23-52% increase in adaptive introgression within shared QTL, suggesting that introgression may be important for parallel evolution. Overall, our results suggest that the same genomic regions contribute to parallel integrated craniofacial phenotypes across lakes. We also highlight the need for more expansive searches for shared QTL when testing for parallel evolution.

evolutionary biology↗

bioRxiv2021

Adaptive introgression and de novo mutations increase access to novel fitness peaks on the fitness landscape during a vertebrate adaptive radiation

Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. However, adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood and processes for surmounting fitness valleys remain controversial. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically novel pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. We leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, estimate genotypic fitness networks, and measure the accessibility of adaptive walks on the fitness landscape. We identified 132 SNPs that were significantly associated with fitness in field enclosures. Six out of the 13 regions most strongly associated with fitness contained differentially expressed genes and fixed SNPs between trophic specialists; one gene (mettl21e) was also misexpressed in lab-reared hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that scale-eating specialists are the most isolated of the three species on these networks. Intriguingly, introgressed and de novo variants reduced fitness landscape ruggedness as compared to standing variation, increasing the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo mutations alter the shape of the fitness landscape, providing key connections in adaptive walks circumventing fitness valleys and triggering the evolution of novelty during adaptive radiation.

evolutionary biology↗

bioRxiv2020

Function of a novel nasal protrusion for oral-shelling within an adaptive radiation of pupfishes

Dietary specialization on hard prey items, such as mollusks and crustaceans, is commonly observed in a diverse array of fish species. Many fish consume these types of prey by crushing the shell to consume the soft tissue within, but a few fishes extricate the soft tissue without breaking the shell using a method known as oral shelling. Oral shelling involves pulling a mollusk from its shell and may be a way to subvert an otherwise insurmountable shell defense. However, the biomechanical requirements and potential adaptations for oral shelling are unknown. Here, we test the hypothesis that a novel nasal protrusion is an adaptation for oral shelling in a durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predicted that a larger nasal protrusion would allow pupfish to consume larger snails. Durophagous pupfish are found within an endemic radiation of pupfish on San Salvador Island, Bahamas. We took advantage of closely related sympatric species and outgroups to test: 1) whether durophagous pupfish shell and consume more snails than other species, 2) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and 3) to determine if nasal protrusion size in parental and hybrid populations increases the maximum diameter snail consumed. We found that durophagous pupfish and their hybrids consumed the most snails, but did not find a strong association between nasal protrusion size and maximum snail size consumed within the parental or F2 hybrid population, suggesting that the size of their novel nasal protrusion does not provide a major benefit in oral shelling. Instead, we suggest that nasal protrusion may increase feeding efficiency, act as a sensory organ, or is a sexually selected trait, and that a strong feeding preference may be most important for oral shelling. Significance StatementSpecialization on hard-shell prey items (i.e. durophagy) is a common dietary niche among fishes. Oral shelling is a rare technique used by some durophagous fish to consume prey items like snails; however, adaptations for oral shelling are still unknown. Here, we document the first evidence of oral shelling in a cyprinodontiform fish, the durophagous pupfish (Cyprinodon brontotheroides), and experimentally test whether its novel nasal protrusion is an adaptation for oral shelling using hybrid feeding trials.

evolutionary biology↗

bioRxiv2020

Conspicuous candidate alleles point to cis-regulatory divergence underlying rapidly evolving craniofacial phenotypes

Developing a mechanistic understanding of genetic variation contributing to variation in complex craniofacial traits is a major goal of both basic and translational research. Investigating closely related species that evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying 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 influencing 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 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 pupfish system as an evolutionary model for craniofacial development.

evolutionary biology↗

bioRxiv2020

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of genetic variants underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. Ancient standing variation from disparate spatial sources was reassembled into new combinations which are under strong selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. This occurred in three stages: first, standing variation associated with feeding behavior swept, then standing variation regulating craniofacial development and pigmentation, and finally de novo variation for craniofacial development. Our results provide clear support for two longstanding hypotheses about adaptive radiation and demonstrate how ancient alleles maintained for millennia in distinct environmental refugia can be assembled into new adaptive combinations. One Sentence SummaryAncient origins of adaptive radiation

evolutionary biology↗

bioRxiv2019

Surprising spatiotemporal stability and frequency-independence across multiple fitness peaks driving adaptive radiation in the wild

The effect of the environment on fitness in natural populations is a fundamental question in evolutionary biology. However, experimental manipulations of environment and phenotype are rare. Thus, the relative importance of the competitive environment versus intrinsic organismal performance in shaping the location, height, and fluidity of fitness peaks and valleys remains largely unknown. We experimentally tested the effect of competitive environment on the fitness landscape driving the evolution of novelty in a sympatric adaptive radiation of a generalist and two trophic specialist pupfishes, a scale-eater and molluscivore, endemic to San Salvador Island, Bahamas. We manipulated phenotypes, by generating 2,611 F4/F5 lab-reared hybrids, and competitive environment, by altering frequencies of rare phenotypes between high- and low-frequency field enclosures, then tracked hybrid survival in two natural lake populations on San Salvador. We found no evidence of frequency-dependent effects on survival fitness landscapes, indicating robustness to the competitive environment. Although survival surfaces favored alternate phenotypes between lakes, joint fitness estimation across lake environments supported multiple fitness peaks for generalist and molluscivore phenotypes and a large fitness valley isolating the most divergent scale-eater phenotype, strikingly similar to a previous independent field experiment. The consistency of this complex fitness landscape across competitive environments, multivariate trait axes, and spatiotemporal heterogeneity provides surprising evidence of stasis in major features of fitness landscapes despite substantial environmental variance, possibly due to absolute biomechanical constraints on diverse prey capture strategies within this radiation. These results challenge competitive speciation theory and highlight the interplay between organism and environment underlying static and dynamic features of the adaptive landscape.

evolutionary biology↗