Evolution Of Traits Research Articles

Parallel phenotypic evolution of two independent cavefish lineages of Astyanax mexicanus (De Filippi, 1854) (Characiformes: Characidae)

Abstract Astyanax mexicanus offers a unique model for studying parallel evolution, with cave-dwelling forms arising from at least two distinct surface lineages. Here, we examined repeated evolution in the two cave-adapted lineages across four phenotypic datasets: (i) meristic data; (ii) ecomorphological data; and geometric morphometric data for (iii) head and (iv) premaxillary bone shape. Additionally, we assessed the association of these phenotypes with their phylogenetic history. Certain traits exhibited evidence of parallel evolution for the cave ecotype across lineages, such as increased maxillary tooth count, reduced lateral line scale count, and shorter ascending process of the premaxillary bone. Geometric morphometric data showed a phenotypic divergence gradient in head shape between cave and surface populations, with the strongest divergence between Sierra de El Abra and surface populations and with less differentiation between surface populations and caves from Sierra de Guatemala and Micos. Cave populations that hybridize with surface populations (e.g. Micos) displayed the greatest overlap with the surface ecotype. There was a similar divergence gradient for premaxillary bone shape, but with weaker differentiation between cave and surface ecotypes. This evidence of repeated evolution in several cave traits emphasizes the significance of selective pressures exerted by the environment on the evolution of cave ecotypes.

Does migration constrain glucocorticoid phenotypes? Testing corticosterone levels during breeding in migratory versus resident birds.

Corticosterone, the main glucocorticoid in birds, is a major mediator of the incredible physiological feat of migration. Corticosterone plays important roles in migration, from preparation to in-flight energy mobilization to refueling, and corticosterone levels often show distinct elevations or depressions during certain stages of the migratory process. Here, we ask whether corticosterone's role in migration shapes its modulation during other life history stages, as is the case with some other phenotypically flexible traits involved in migration. Specifically, we use a global dataset of corticosterone measures to test whether birds' migratory status (migrant versus resident) predicts corticosterone levels during breeding. Our results indicate that migratory status predicts neither baseline nor stress-induced corticosterone levels in breeding birds; despite corticosterone's role in migration, we find no evidence that migratory corticosterone phenotypes carry over to breeding. We encourage future studies to continue to explore corticosterone in migrants versus residents across the annual cycle. Additionally, future efforts should aim to disentangle the possible effects of environmental conditions and migratory status on corticosterone phenotypes; potentially fruitful avenues include focusing on regions where migrants and residents overlap during breeding. Overall, insights from work in this area could demonstrate whether migration shapes traits during other important life stages, identify tradeoffs or limitations associated with the migratory lifestyle, and ultimately shed light on the evolution of flexible traits and migration.

Digest: Sexually selected traits can affect individual fitness and trait evolution in a butterfly species.

Wedell and Kemp ([2024]. Examined the importance of female sexual preferences for male UV reflectance on offspring viability and the evolution of male traits in the butterfly Eurema hecabe. Female preferences were found to have multiple consequences, including increased trait value, higher offspring viability, and reduced mutational load. These findings highlight that female sexual preferences for specific male traits can also have further consequences for individual fitness and evolution of specific morphological characteristics.

Fast mvSLOUCH: Multivariate Ornstein–Uhlenbeck‐based models of trait evolution on large phylogenies

Abstract The PCMBase R package is a powerful computational tool that enables efficient calculations of likelihoods for a wide range of phylogenetic Gaussian models. Taking advantage of it, we redesigned the R package mvSLOUCH. Here, we demonstrate how the new version of the package can be used to thoroughly examine the evolution and adaptation of traits in a large dataset of 1252 vascular plants through the use of multivariate Ornstein–Uhlenbeck processes. The results of our analysis demonstrate the ability of the modelling framework to distinguish between various alternative hypotheses regarding the evolution of functional traits in angiosperms.

Mismatch Resistance and the Problem of Evolutionary Novelty

AbstractIn evolutionary medicine and other related fields, the concept of evolutionary mismatch is used to explain phenomena whereby traits reduce in adaptive value and eventually become maladaptive as the environment changes. This article argues that there is a similar problem of persistent adaptivity—what has been called the problem of evolutionary novelty—and it introduces the concept of mismatch resistance in order to explain phenomena whereby traits retain their adaptive value in novel environments that are radically different from the organisms’ environment of evolutionary adaptedness (EEA). The possible role of variability selection in the evolution of mismatch-resistant traits is discussed, and it is suggested that mismatch resistance provides a useful tool for making progress on certain issues related to evolutionary theory, such as the modularity debate, cases of adaptivity outside of organisms’ ancestral environment, and the viability of naturalism as an overarching philosophical framework for understanding the natural world.

A multiscale analysis of coralline algae Lithophylloideae (Corallinophycidae, Rhodophyta) shedding new light on understanding cryptic diversity

Cryptic diversity abounds in many biological species, posing challenges to our understanding of biological diversity, conservation and management. Taking the common coralline algae, the subfamily Lithophylloideae as an illustration, this study delved into the implications of cryptic diversity through global-level phylogenetic and geographical analysis based upon Lithophylloideae molecular data worldwide, as well as a multi-locus time-calibrated phylogeny to elucidate their possible evolutionary process. The multiscale analysis revealed the polyphyly in current concept of the genus Lithophyllum. Geographic isolation resulting from the Tethys terminal event (TTE) has led to two distinct distribution regions for this so-called cosmopolitan genus: one regionally distributed along European coasts/Mediterranean that should include the taxonomical Lithophyllum; others widely distributed, particularly among pan-tropic waters, suggesting at least five groups to be rediscovered within the subfamily Lithophylloideae. Meanwhile, the cryptic genus Titanoderma, lacking morphological identification features with Lithophyllum, exhibited differences in distribution and evolutionary patterns consistent with their ecological habits, thus supporting their separation. This study provided useful hints for cryptic diversity, which advocated an integrative thinking to investigating global cryptic diversity and exploring the broad linkages between phylogenetic relationships and evolutionary origin, biogeography, morphological and ecological traits to achieve a more comprehensive understanding of biodiversity.

A comparative approach for life history and functional response demonstrates similar survival strategies for Trichogramma evanescens and T. pintoi.

Egg parasitoids are important biological control agents of lepidopteran pests of agricultural crops. Trichogramma evanescens Westwood and T. pintoi Voegele (Hymenoptera: Trichogrammatidae) are egg parasitoids with worldwide importance. The parasitoid selection necessitates comparative assessment of the life table traits and functional response analysis to provide insights into their effectiveness in pest control. In this study, we examined theirlife table traits including survivorship and reproductivity, and functional response and associated parameters i.e., attack coefficient and handling time. Life table parameters, using age-stage, two-sex theory, revealed similar survival and reproductive strategies for both species. For example, the female longevity, oviposition days and fecundity did not differ between both species. Exceptionally, the male longevity of T. evanescens was shorter than that of T. pintoi. The population growth parameters such as gross reproductive rate (GRR), net reproductive rate (R0), intrinsic rate of increase (r), finite rate of increase (λ), and mean generation time (T) did not differ between species. The polynomial logistic regression yielded a type III functional response and a non-linear least square analysis revealed different attack coefficient and similar handling time. However, their parasitism rate differed between the lowest (five eggs) and highest (80 eggs) initial host egg densities such that T. evanescens had a lower parasitism rate at the lowest density and higher parasitism rate at the highest density. The similarity in survival strategies and minor differences in host handling of both parasitoids are discussed in terms of relevance to applied biological control applications and evolutionary traits. © 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Virological characteristics of the SARS-CoV-2 Omicron EG.5.1 variant.

In middle to late 2023, a sublineage of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron XBB, EG.5.1 (a progeny of XBB.1.9.2), is spreading rapidly around the world. We performed multiscale investigations, including phylogenetic analysis, epidemic dynamics modeling, infection experiments using pseudoviruses, clinical isolates, and recombinant viruses in cell cultures and experimental animals, and the use of human sera and antiviral compounds, to reveal the virological features of the newly emerging EG.5.1 variant. Our phylogenetic analysis and epidemic dynamics modeling suggested that two hallmark substitutions of EG.5.1, S:F456L and ORF9b:I5T are critical to its increased viral fitness. Experimental investigations on the growth kinetics, sensitivity to clinically available antivirals, fusogenicity, and pathogenicity of EG.5.1 suggested that the virological features of EG.5.1 are comparable to those of XBB.1.5. However, cryo-electron microscopy revealed structural differences between the spike proteins of EG.5.1 and XBB.1.5. We further assessed the impact of ORF9b:I5T on viral features, but it was almost negligible in our experimental setup. Our multiscale investigations provide knowledge for understanding the evolutionary traits of newly emerging pathogenic viruses, including EG.5.1, in the human population.

Understanding the Genetic Basis of Variation in Meiotic Recombination: Past, Present, and Future.

Meiotic recombination is a fundamental feature of sexually reproducing species. It is often required for proper chromosome segregation and plays important role in adaptation and the maintenance of genetic diversity. The molecular mechanisms of recombination are remarkably conserved across eukaryotes, yet meiotic genes and proteins show substantial variation in their sequence and function, even between closely related species. Furthermore, the rate and distribution of recombination shows a huge diversity within and between chromosomes, individuals, sexes, populations, and species. This variation has implications for many molecular and evolutionary processes, yet how and why this diversity has evolved is not well understood. A key step in understanding trait evolution is to determine its genetic basis-that is, the number, effect sizes, and distribution of loci underpinning variation. In this perspective, I discuss past and current knowledge on the genetic basis of variation in recombination rate and distribution, explore its evolutionary implications, and present open questions for future research.

Chromosome-level genome assembly of Helwingia omeiensis: the first genome in the family Helwingiaceae

Helwingia, a shrub of the monotypic cosmopolitan family Helwingiaceae, is distinguished by its inflorescence, in which flowers are borne on the midrib of the leaf—a trait not commonly observed in related plant families. Previous studies have investigated the development of this unusual structure using comparative anatomical methods. However, the scarcity of genomic data has hindered our understanding of the origins and evolutionary history of this uncommon trait at the molecular level. Here, we report the first high-quality genome of the family Helwingiaceae. Assembled using HiFi sequencing and Hi-C technologies, the genome of H. omeiensis is anchored to 19 chromosomes, with a total length of 2.75 Gb and a contig N50 length of 6.78 Mb. The BUSCO completeness score of the assembled genome was 98.2%. 53,951 genes were identified, of which 99.7% were annotated in at least one protein database. The high-quality reference genome of H. omeiensis provides an essential genetic resource and sheds light on the phylogeny and evolution of specific traits in the family Helwingiaceae.

A mathematical description of fossilization.

Fossils constitute an inestimable archive of past life on the Earth. However, the stochastic processes driving decay and fossilization and overwhelmingly distorting this archive, are challenging to interpret. Consequently, concepts of exceptional or poor preservation are often subjective or arbitrarily defined. Here, we offer an alternative way to think about fossilization. We propose a mathematical description of decay and fossilization relying on the change in the relative frequency and characteristics of biogenic objects (e.g. atoms, functional groups, molecules, body parts and organisms) within an organism-fossil system. This description partitions taphonomic changes into three categories: gain, loss and alteration of state. Although the changes undergone by organisms through decay, preservation and alteration vary a lot for different organisms under different conditions, we provide a unified formalism which can be applied directly in the comparison of different assemblages, experiments and fossils. Our expression is closely related to George R. Price's famous equation for the change in evolutionary traits and can be adapted to the study of palaeontological systems and many others.

Correlated evolution of conspicuous colouration and burrowing in crayfish.

Conspicuous colours have fascinated biologists for centuries, leading to research on the evolution and functional significance of colour traits. In many cases, research suggests that conspicuous colours are adaptive and serve a function in sexual or aposematic signalling. In other cases, a lack of evidence for the adaptive value of conspicuous colours garners interest from biologists, such as when organisms that live underground and are rarely exposed to the surface are nevertheless colourful. Here, we use phylogenetic comparative methods to investigate colour evolution throughout freshwater crayfishes that vary in burrowing ability. Within the taxa we analysed, conspicuous colours have evolved independently over 50 times, and these colours are more common in semi-terrestrial crayfishes that construct extensive burrows. The intuitive but not evolutionarily justified assumption when presented with these results is to assume that these colours are adaptive. But contrary to this intuition, we discuss the hypothesis that colouration in crayfish is neutral. Supporting these ideas, the small population sizes and reduced gene flow within semi-terrestrial burrowing crayfishes may lead to the fixation of colour-phenotype mutations. Overall, our work brings into question the traditional view of animal colouration as a perfectly adapted phenotype.

The significance of follow-up in patients with dysmorphic features: a case from clinical practice

Background. Kabuki syndrome is a rare disorder, that is characterized by typical facial dysmorphism, hypotonia, delay in intellectual and motor development. Case report. We present a case of a girl in whom polycystic left kidney was prenatally established. Born prematurely in 37 weeks by C section due to oligohydramnios. After birth, atresia of the anus with fistula, cysts in the left and reduced dimensions of the right kidney, were further established. A normal female karyotype was found and targeted sequencing analysis was conducted on a panel of 81 genes associated with renal abnormalities – no pathogenic variants were detected. The child was then followed up by its general practitioner. At the age of 2 years, she was again referred for genetic counseling, which revealed the following dysmorphic signs – long eye palpebral fissuras with ectropion of the lower eyelid, sparsed lateral eyebrows, depression of the nasal bridge, brachydactyly and others characteristic of Kabuki’s syndrome. The conducted molecular genetic analysis confirmed the clinical diagnosis – a likely pathogenic variant in the KMT2D gene was established. Conclusions. Certain pathognomonic facial may not present at birth and only appear after a few years. Therefore, monitoring of the evolution of dysmorphic traits is required.

Resting Metabolic Rate Does Not Predict Peak Metabolic Rate in the Glanville Fritillary Butterfly.

Peak metabolic rate reflects maximal performance and may have direct fitness consequences, whereas resting metabolic rate (RMR) represents the maintenance cost of the whole animal. These traits may be linked, which has significant implications for the evolution of both traits. In vertebrates, a positive correlation between RMR and aerobic capacity has been proposed to explain the origin of endothermy. However, as studies on the relationship between RMR and aerobic capacity have focused on vertebrates, we know much less about these traits in ectothermic insects. I measured RMR in the Glanville fritillary butterfly (Melitaea cinxia) using two configurations: one optimized for measuring flight metabolic rate and the other optimized for RMR. The relationship between RMR and body mass was similar for the two configurations. Body mass explained 82% of the variation in RMR when it was measured using the "flight" configuration at 32°C, and 91% when using the "rest" configuration at 23°C. The Q10 coefficient calculated based on the two RMR measurements was 2.8. Mass-independent RMR was positively correlated between measurements obtained using the two instrument configurations. However, neither measure of RMR was correlated with peak metabolic rate, which indicates that RMR cannot be used as a surrogate measure for aerobic capacity in the Glanville fritillary. Ectothermic insects may be able to combine high metabolic capacity with no apparent increase in maintenance cost. Even though RMR is among the most frequently measured physiological variables, it may have limited predictive power when it comes to questions related to activity or aerobic capacity, or in the case of butterflies, flight performance.

The macro-eco-evolutionary interplay between dispersal, competition and landscape structure in generating biodiversity.

Theory links dispersal and diversity, predicting the highest diversity at intermediate dispersal levels. However, the modulation of this relationship by macro-eco-evolutionary mechanisms and competition within a landscape is still elusive. We examine the interplay between dispersal, competition and landscape structure in shaping biodiversity over 5 million years in a dynamic archipelago landscape. We model allopatric speciation, temperature niche, dispersal, competition, trait evolution and trade-offs between competitive and dispersal traits. Depending on dispersal abilities and their interaction with landscape structure, our archipelago exhibits two 'connectivity regimes', that foster speciation events among the same group of islands. Peaks of diversity (i.e. alpha, gamma and phylogenetic), occurred at intermediate dispersal; while competition shifted diversity peaks towards higher dispersal values for each connectivity regime. This shift demonstrates how competition can boost allopatric speciation events through the evolution of thermal specialists, ultimately limiting geographical ranges. Even in a simple landscape, multiple intermediate dispersal diversity relationships emerged, all shaped similarly and according to dispersal and competition strength. Our findings remain valid as dispersal- and competitive-related traits evolve and trade-off; potentially leaving identifiable biodiversity signatures, particularly when trade-offs are imposed. Overall, we scrutinize the convoluted relationships between dispersal, species interactions and landscape structure on macro-eco-evolutionary processes, with lasting imprints on biodiversity.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Coinfection accelerates transmission to new hosts despite no effects on virulence and parasite growth.

One of the fundamental aims of ecological, epidemiological and evolutionary studies of host-parasite interactions is to unravel which factors affect parasite virulence. Theory predicts that virulence and transmission are correlated by a trade-off, as too much virulence is expected to hamper transmission owing to excessive host damage. Coinfections may affect each of these traits and/or their correlation. Here, we used inbred lines of the spider mite Tetranychus urticae to test how coinfection with T. evansi impacted virulence-transmission relationships at different conspecific densities. The presence of T. evansi on a shared host did not change the relationship between virulence (leaf damage) and the number of transmitting stages (i.e. adult daughters). The relationship between these traits was hump-shaped across densities, both in single and coinfections, which corresponds to a trade-off. Moreover, transmission to adjacent hosts increased in coinfection, but only at low T. urticae densities. Finally, we tested whether virulence and the number of daughters were correlated with measures of transmission to adjacent hosts, in single and coinfections at different conspecific densities. Traits were mostly independent, meaning that interspecific competitors may increase transmission without affecting virulence. Thus, coinfections may impact epidemiology and parasite trait evolution, but not necessarily the virulence-transmission trade-off.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Complex patterns of gene flow and convergence in the evolutionary history of the spiral-horned antelopes (Tragelaphini)

The Tragelaphini, also known as spiral-horned antelope, is a phenotypically diverse mammalian tribe comprising a single genus, Tragelaphus. The evolutionary history of this tribe has attracted the attention of taxonomists and molecular geneticists for decades because its diversity is characterised by conflicts between morphological and molecular data as well as between mitochondrial, nuclear and chromosomal DNA. These inconsistencies point to a complex history of ecological diversification, coupled by either phenotypic convergence or introgression. Therefore, to unravel the phylogenetic relationships among spiral-horned antelopes, and to further investigate the role of divergence and gene flow in trait evolution, we sequenced genomes for all nine accepted species of the genus Tragelaphus, including a genome each for the highly divergent bushbuck lineages (T. s. scriptus and T. s. sylvaticus). We successfully reconstructed the Tragelaphus species tree, providing genome-level support for the early Pliocene divergence and monophyly of the nyala (T. angasii) and lesser kudu (T. imberbis), the monophyly of the two eland species (T. oryx and T. derbianus) and, importantly, the monophyly of kéwel (T. s. scriptus) and imbabala (T. s. sylvaticus) bushbuck. We found strong evidence for gene flow in at least four of eight nodes on the species tree. Among the six phenotypic traits assessed here, only habitat type mapped onto the species tree without homoplasy, showing that trait evolution was the result of complex patterns of divergence, introgression and convergent evolution.

Do flower-colonizing microbes influence floral evolution? A test with fast-cycling Brassica.

Pollinators are thought to be the main drivers of floral evolution. Flowers are also colonized by abundant communities of microbes that can affect the interaction between plants and their pollinators. Very little is known, however, about how flower-colonizing microbes influence floral evolution. Here we performed a 6-generation experimental evolution study using fast-cycling Brassica rapa, in which we factorially manipulated the presence of pollinators and flower microbes to determine how pollinators and microbes interact in driving floral evolution. We measured the evolution of 6 morphological traits, as well as the plant mating system and flower attractiveness. Only one of the 6 traits (flower number) evolved in response to pollinators, while microbes did not drive the evolution of any trait, nor did they interact with pollinators in driving the evolution of morphological traits. Moreover, we did not find evidence that pollinators or microbes affected the evolution of flower attractiveness to pollinators. However, we found an interactive effect of pollinators and microbes on the evolution of autonomous selfing, a trait that is expected to evolve in response to pollinator limitations. Overall, we found only weak evidence that microbes mediate floral evolution. However, our ability to detect an interactive effect of pollinators and microbes might have been limited by weak pollinator-mediated selection in our experimental setting. Our results contrast with previous (similar) experimental evolution studies, highlighting the susceptibility of such experiments to drift and to experimental artefacts.

Behavioural changes in aposematic Heliconius melpomene butterflies in response to their predatory bird calls

Prey-predator interactions have resulted in the evolution of many anti-predatory traits. One of them is the ability for prey to listen to predators and avoid them. Although prey anti-predatory behavioural responses to predator auditory cues are well described in a wide range of taxa, studies on whether butterflies change their behaviours in response to their predatory calls are lacking. Heliconius butterflies are unpalatable and form Müllerian mimicry rings as morphological defence strategies against their avian predators. Like many other butterflies in the Nymphalidae family, some Heliconius butterflies possess auditory organs, which are hypothesized to assist with predator detection. Here we test whether Heliconius melpomene change their behaviour in response to their predatory bird calls by observing the behaviour of male and female H. m. plessini exposed to calls of Heliconius avian predators: rufous-tailed jacamar, migratory Eastern kingbird, and resident tropical kingbird. We also exposed them to the calls of the toco toucan, a frugivorous bird as a control bird call, and an amplified greenhouse background noise as a noise control. We found that individuals changed their behaviour in response to jacamar calls only. Males increased their walking and fluttering behaviour, while females did not change their behaviour during the playback of the jacamar call. Intersexual behaviours like courtship, copulation, and abdomen lifting did not change in response to bird calls. Our findings suggest that despite having primary predatory defences like toxicity and being in a mimicry ring, H. m. plessini butterflies changed their behaviour in response to predator calls. Furthermore, this response was predator specific, as H. m. plesseni did not respond to either the Eastern kingbird or the tropical kingbird calls. This suggests that Heliconius butterflies may be able to differentiate predatory calls, and potentially the birds associated with those calls.

Mutations in the albinism gene oca2 alter vision-dependent prey capture behavior in the Mexican tetra.

Understanding the phenotypic consequences of naturally occurring genetic changes, as well as their impact on fitness, is fundamental to understanding how organisms adapt to an environment. This is critical when genetic variants have pleiotropic effects, as determining how each phenotype impacted by a gene contributes to fitness is essential to understand how and why traits have evolved. A striking example of a pleiotropic gene contributing to trait evolution is the oca2 gene, coding mutations in which underlie albinism and reductions of sleep in the blind Mexican cavefish, Astyanax mexicanus. Here, we characterize the effects of mutations in the oca2 gene on larval prey capture. We find that when conspecific surface fish with engineered mutations in the oca2 allele are hunting, they use cave-like, wide angle strikes to capture prey. However, unlike cavefish or surface fish in the dark, which rely on lateral line mediated hunting, oca2 mutant surface fish use vision when striking at prey from wide angles. Finally, we find that while oca2 mutant surface fish do not outcompete pigmented surface siblings in the dark, pigmented fish outcompete albino fish in the light. This raises the possibility that albinism is detrimental to larval feeding in a surface-like lighted environment, but does not have negative consequences for fish in cave-like, dark environments. Together, these results demonstrate that oca2 plays a role in larval feeding behavior in A. mexicanus. Further, they expand our understanding of the pleiotropic phenotypic consequences of oca2 in cavefish evolution.