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Biology subjects

Bentley, B. P.

Publications and source records attributed to Bentley, B. P..

7 recordsLinked to original sources

Phenological plasticity provides limited resilience to climate warming in a sea turtle species with temperature-dependent sex determination

Anthropogenic climate change is threatening global biodiversity, with sea turtles particularly vulnerable as offspring sex and developmental success are strongly influenced by incubation temperature. Behavioral plasticity, including the seasonal distribution of reproductive output, may provide short-term mechanisms for mitigating these impacts. Here, we investigated season-wide hatchling sex ratios and emergence success in a small population of green turtles (Chelonia mydas), tracking individual females across their nesting seasons. Sex ratios varied markedly through the nesting season, with later nests producing a greater proportion of male hatchlings. Moreover, sex ratios were relatively consistent among nests laid by individual females. Overall, females producing more nests over a season also produced more male offspring, suggesting that both nesting phenology and reproductive output influence individual contributions to future population demographics. Mechanistic models indicate that hatchling sex ratios have trended towards female-biased ratios (>80% female) over the past 50 years, and are projected to approach complete feminization by 2100 under continued warming. Although emergence success currently remains high (>85%), it is predicted to decline sharply after mid-century, with viable hatchling production falling to [~]30% by the end of the century. Models further show that maintaining contemporary sex ratios and emergence success will require unrealistically large delays in nesting phenology, and that even extreme shifts in phenology become ineffective by 2100. Together, these findings demonstrate that individual females can increase male hatchling production by nesting later and producing more nests, but behavioral plasticity alone is unlikely to offset the accelerating impacts of climate change on this population.

ecology↗

Genomic indicators of risk and resilience in global leatherback turtle populations

Understanding the drivers of genomic health and their consequences for population viability is often overlooked but potentially important to effective conservation amidst the biodiversity crisis of the Anthropocene. Leatherback turtle (Dermochelys coriacea) populations have declined globally due to anthropogenic factors, with some populations losing over 90% of their abundance over the past 30-50 years. While conservation efforts have been successful in stabilizing some populations, others continue to decline, and the reasons for these differential trajectories remain unclear. To assess how recent demographic factors, such as population size and decline, influence population genomic health, we combined population monitoring information with medium depth whole-genome and reduced representation resequencing data from globally representative populations. We found that small-stable populations have lower genomic diversity and higher inbreeding than large declining populations, reflecting prolonged small population sizes and limited gene flow. Yet, small-stable populations also show evidence of deleterious allele purging, suggesting genetic resilience. This, combined with lack of detectable genomic erosion over the study period, provides hope for potential recovery of healthy leatherback populations provided that anthropogenic threats are effectively mitigated. However, potential time lags and possible recent increases in inbreeding among close relatives in recently declined populations warrant continued monitoring and assessment. Genomic and abundance-based metrics were less aligned following rapid population declines, emphasizing the different timescales of the evolutionary and demographic processes they reflect, respectively, and the strength in their complementary, integrative use for extinction risk assessments. This also supports that it is not too late to turn the tide for recently declined leatherback populations and that continued investment in conservation efforts and threat reductions are warranted. Collectively, our results highlight how recent and historical demography shapes current genomic health and recovery potential in leatherback turtles, aids understanding of current risks and informs future conservation and management strategies.

ecology↗

Assessing climate adaptation among Canada lynx (Lynx canadensis) populations at the trailing edge

Species must acclimate, shift their distributions, or adapt in place in response to anthropogenic climate change. Populations at low-latitude trailing edges of species distributions typically experience thermal conditions closest to the upper limit of their thermoregulatory capacity. Landscape and functional genomic approaches provide quantitative measures of risk and adaptive capacity which can inform and prioritize conservation actions. Using low-coverage whole genomes from Canada lynx (Lynx canadensis), we characterized population genomic structure and identified putatively adaptive loci using genotype-environment association analyses across the eastern extent of their distribution. We detected genetic breaks across two previously identified biogeographical barriers, the St. Lawrence River and the Strait of Belle Isle, and found relatively high genome-wide diversity in the Maine population at the southern trailing edge, suggesting a reservoir of warm-adapted variation. We identified 759 loci from 329 genes as putatively adaptive, many associated with temperature during warm and dry periods, and functionally enriched in photoreception, circadian entrainment, and temperature regulation. We identified ten putatively adaptive genes linked to epilepsy, presenting candidate genes underlying reports of idiopathic epilepsy in captive populations of closely related lynx species (L. lynx and L. pardinus). Genetic offset showed lynx in Western Newfoundland, and the Gaspe Peninsula in Quebec are at the greatest risk of maladaptation under future conditions. If gene flow allows, introgression of climate-adapted loci from the trailing-edge may benefit regional populations under future climates. Together, these findings demonstrate the conservation value of locally adapted range-edge populations.

genomics↗

DNA methylation reveals evolved buffering responses to climate-driven sex ratio skew in sea turtles

Species with temperature-dependent sex determination (TSD), including all sea turtles which produce females at warmer temperatures, face projections of demographic collapse under climate-driven sex ratio skews. However, the accuracy of such predictions remains uncertain, as current models rely heavily on indirect sex ratio proxies due to the lack of a scalable, non-invasive method for sexing hatchlings. Through whole methylome sequencing, we identified 777 sex-associated DNA methylation markers from blood samples of sex-verified loggerhead turtle (Caretta caretta) hatchlings incubated at three controlled temperatures. Applying these markers to a large-scale field experiment showed that classic nest temperature-based models overestimated female production by an average of up to 60.2%, suggesting the presence of evolved buffering mechanisms against thermal effects on sex determination. Our findings highlight the need to revise climate-driven sex ratio forecasts with empirical field data, such as methylation-based assessments, to better understand and safeguard the hidden resilience of vulnerable TSD species.

zoology↗

Adaptation to warm environments with a fast pace of life in a marine predatory snail

Understanding how latitudinal temperature variation shapes local adaptation of life history strategies is crucial for predicting future responses to warming. Contrasting predictive frameworks explain how growth and other life history traits may respond to differing selective pressures across latitude. However, these frameworks have rarely been explored within the context of fluctuating environmental temperatures across longer (i.e., seasonal) time scales experienced in nature. Furthermore, consequences of growth differences for other aspects of fitness, including reproductive output, remain unclear. Here, we conducted a long-term (17-month) simulated reciprocal transplant experiment to examine local adaptation in two populations of the predatory marine snail Urosalpinx cinerea separated by 8.6{degrees} latitude (1000 km). We reared F1 offspring under two seasonally fluctuating temperature regimes ("warm" and "cold", simulating field thermal conditions experienced by low and high latitude populations, respectively), quantifying temporal patterns in growth, maturation, and reproductive output. We identified striking divergence in life-history strategies between populations in the warm regime, with offspring from the low latitude population achieving greater growth in their first year, and high reproductive output coupled with reduced growth in their second year. In contrast, the high latitude population grew slower in their first year, but eventually attained larger sizes in their second year, at the expense of reduced reproductive output. Responses were consistent with this in the cold regime, although growth and reproductive output was reduced in both populations. Our data provides support for adaptive divergence across latitude consistent with the Pace-of-Life hypothesis, with the low latitude population selected for a fast-paced life characterized by rapid development and early reproduction. In contrast, the high latitude population exhibited slower growth and delayed maturation. Our results highlight the potential limitations of short-term comparisons of growth without considering processes over longer time scales that may exhibit seasonal temperature variation and ontogenetic shifts in energy allocation and imply a radical reshaping of physiological performance and life history traits across populations under climate change.

ecology↗

Haplotype-resolved reference genomes of the sea turtle clade unveil ultra-syntenic genomes with hotspots of divergence

BackgroundReference genomes for the entire sea turtle clade have the potential to reveal the genetic basis of traits driving the ecological and phenotypic diversity in these ancient and iconic marine species. Furthermore, these genomic resources can support conservation efforts and deepen our understanding of their unique evolution. ResultsWe present haplotype-resolved, chromosome-level reference genomes and high-quality gene annotations for five sea turtle species. This completes the catalog of reference genomes of the entire sea turtle clade when combined with our previously published reference genomes. Our analysis reveals remarkable genome synteny and collinearity across all species, despite the clades origin dating back more than 60 million years. Regions of high interspecific genetic distance and intraspecific genetic diversity are consistently clustered in genomic hotspots, which are enriched with genes coding for immune response proteins, olfactory receptors, zinc fingers, and G-protein-coupled receptors. These hotspot regions may offer insights into the genetic mechanisms driving phenotypic divergence among species, and represent areas of significant adaptive potential. Ancient demographic analysis revealed a synchronous population expansion among sea turtle species during the Pleistocene, with varying magnitudes of demographic change, likely shaped by their diverse ecological adaptations, and biogeographic contexts. ConclusionsOur work provides genomic resources for exploring genetic diversity, evolutionary adaptations, and demographic histories of sea turtles. We outline genomic regions with increased diversity, linked to immune response, sensory evolution, and adaptation to varying environments that have historically been subject to strong diversifying selection, and likely will underpin sea turtles responses to future environmental change. These reference genomes can assist conservation by providing insights into the demographic and evolutionary processes that sustain and threaten these iconic species.

genomics↗

Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of non-collinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared to other reptiles, and harbor a higher genetic load compared to green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage. Statement of significanceSea turtle populations have undergone recent global declines. We analyzed de novo assembled genomes for both extant sea turtle families through the Vertebrate Genomes Project to inform their conservation and evolutionary biology. These highly conserved genomes were differentiated by localized gene-rich regions of divergence, particularly within microchromosomes, suggesting that these genomic elements play key functional roles in the evolution of sea turtles and possibly other vertebrates. We further demonstrate that dissimilar evolutionary histories impact standing genomic diversity and genetic load, and are critical to consider when using these metrics to assess adaptive potential and extinction risk. Our results also demonstrate how reference genome quality impacts inferences of comparative and conservation genomics analyses that need to be considered in their application.

genomics↗