Multisensory integration (MSI) combines information from more than one sensory modality to elicit behaviors distinct from unisensory behaviors. MSI is best understood in animals with complex brains and specialized centers for parsing sensory information, but the dispersive larvae of sessile marine invertebrates utilize multimodal environmental sensory stimuli to base irreversible settlement decisions on, and most lack complex brains. Here, we examined the sensory determinants of settlement in actinula larvae of the hydrozoan Ectopleura crocea (Cnidaria), which possess a diffuse nerve net. A factorial settlement study revealed that photo-, chemo-, and mechano-sensory cues each influence the settlement response, which was complex and dependent on specific combinations of cues, therefore indicating MSI. Mechanosensory cues either inhibited or enhanced settlement rates depending on the presence or absence of chemical and light cues in the environment. Sensory gene expression over development peaked with developmental competence to settle, which in actinulae, requires cnidocyte discharge. Transcriptome analyses also highlighted several deep homological links between cnidarian and bilaterian mechano- chemo- and photo-sensory pathways. Fluorescent in situ hybridization studies of candidate transcripts suggested cellular partitioning of sensory function among the few cell types that comprise the actinula nervous system, where ubiquitous polymodal sensory neurons with putative chemo- and photo-sensitivity interface with mechanoreceptive cnidocytes. We propose that a simple multisensory processing circuit, involving polymodal chemo/photosensory neurons and mechanoreceptive cnidocytes, is sufficient to explain MSI in actinulae settlement. Our study demonstrates that MSI is not exclusive to complex brains, but likely predated and contextualized their evolution.
Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere dynamics driven by thermal stress are of particular interest during the early post-natal stages of altricial birds because nestlings quickly shift from being ectothermic to poikilothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but investigations within species that transition from ectothermy to endothermy are lacking. Also, ambient temperature influences parental brooding behavior, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves, and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that correspond to three different thermoregulatory stages (ectothermic, poikilothermic and endothermic respectively); we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (poikilothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at five days old) compared to controls. Lower brooding effort was associated with shorter telomeres in 12 day old nestlings. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behavior during growth.
The genomics revolution continues to change how ecologists and evolutionary biologists study the evolution and maintenance of biodiversity. It is now easier than ever to generate large molecular data sets consisting of hundreds to thousands of independently evolving nuclear loci to estimate a suite of evolutionary and demographic parameters. However, any inferences will be incomplete or inaccurate if incorrect taxonomic identities and perpetuated throughout the analytical pipeline. Due to decades of research and comprehensive online databases, sequencing of mitochondrial DNA (mtDNA), chloroplast DNA (cpDNA) and select nuclear genes can provide researchers with a cost effective and simple means to verify the species identity of samples prior to subsequent phylogeographic and population genomic analysis. The addition of these sequences to genomic studies can also shed light on other important evolutionary questions such as explanations for gene tree-species tree discordance, species limits, sex-biased dispersal patterns, and mtDNA introgression. Although the mtDNA and cpDNA genomes often should not be used exclusively to make historical inferences given their well-known limitations, the addition of these data to modern genomic studies adds little cost and effort while simultaneously providing a wealth of useful data that can have significant implications for both basic and applied research.
Traditional agrosystems, where humans, crops and microbes have coevolved over long periods, can serve as models to understand the eco-evolutionary determinants of disease dynamics and help the engineering of durably resistant agrosystems. Here, we investigated the genetic and phenotypic relationship between rice (Oryza sativa) landraces and their rice blast pathogen (Pyricularia oryzae) in the traditional Yuanyang terraces of flooded rice paddies in China, where rice landraces have been grown and bred over centuries without significant disease outbreaks. Analyses of genetic subdivision revealed that indica rice plants clustered according to landrace names. Three new diverse lineages of rice blast specific to the Yuanyang terraces coexisted with lineages previously detected at the worldwide scale. Population subdivision in the pathogen population did not mirror pattern of population subdivision in the host. Measuring the pathogenicity of rice blast isolates on landraces revealed generalist life histories. Our results suggest that the implementation of disease control strategies based on the emergence or maintenance of a generalist lifestyle in pathogens may sustainably reduce the burden of disease in crops.
Male reproductive competition can select for condition-dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male’s current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analyzed photographs collected during natural (n=144) and anesthetized conditions (n=38) to understand variability in male and female chest redness, and we used chest skin biopsies (n=38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within-individual range in redness under natural conditions. These sex differences were reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patters between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or estrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high-altitude environment of geladas.
During the Late Pleistocene, major parts of North America were periodically covered by ice sheets. However, there are still open questions about whether ice-free refugia were present in the Alexander Archipelago along the Southeast (SE) Alaska coast during the Last Glacial Maximum (LGM). Numerous subfossils have been recovered from caves in SE Alaska, including American black (Ursus americanus) and brown (U. arctos) bears, which today are found in the Alexander Archipelago but are genetically distinct from mainland bear populations. Hence, these bear species offer an ideal system to investigate long-term occupation, potential refugial survival, and lineage turnover. Here we present genetic analyses based on 99 new complete mitochondrial genomes from ancient and modern brown and black bears spanning the last ~45,000 years. Black bears form two SE Alaskan subclades that diverged >100,00 years ago, one preglacial and one postglacial. All postglacial ancient brown bears are closely related to modern bears in the archipelago, while a single preglacial brown bear is found in a distantly related clade. A hiatus in the bear subfossil record around the LGM and the deep split of their pre- and post-glacial subclades fail to support a hypothesis of continuous occupancy in SE Alaska throughout the LGM for either species. Our results are consistent with an absence of refugia along the SE Alaska coast, but indicate that vegetation quickly expanded after deglaciation, allowing bears to recolonize the area after a short-lived LGM peak.
Telomerase activity and telomere maintenance in certain somatic cells of human adults support the proliferative capacity of these cells and thus contribute to their regenerative potential, and telomerase activity and telomere length are commonly considered lifespan predictors. Eusocial insects provide excellent models for aging research based on their extraordinary caste-related lifespan differences that contradict the typical mammalian fecundity/lifespan trade-off. Telomerase activity is upregulated in the reproductive, long-lived individuals of eusocial insects such as queens and kings, and telomerase activity may act as a key factor in their extended longevity. But, as documented by the presence of telomerase in somatic tissues of numerous invertebrate and vertebrate species, the connection between telomerase activity and the predicted lifespan is not clear. Here, I ask whether somatic telomerase activity in eusocial reproductives may serve its non-canonical function to protect its individuals against the metabolic stress due to reproduction and reflect a more common phenomenon among species. Here, I propose a hypothesis that the presence of telomerase activity in somatic cells reflects a different reproduction strategy of species.
In organisms reproducing sexually, speciation occurs when increasing divergence results in pre- or post-zygotic reproductive isolation between lineages. Studies focusing on reproductive isolation origin in early stages of speciation are common. Many rely on indirect measures of introgression providing limited information on the genomic architecture of reproductive isolation maintenance in the long term. This study focuses on direct measures of introgression between two species in a late stage of speciation. We used ddRADseq genotyping in a natural hybrid zone between Podarcis bocagei and P. carbonelli to examine admixture extent, estimate effective selection, analyse hybrid zone stability, and assess variation in selection against introgression across the genome. Hybridization was confirmed the narrow and bimodal hybrid zone demonstrating the existence of strong mechanisms of reproductive isolation. Simulations suggested that simple premating barriers were not enough to explain the observed distribution of admixture classes, pointing out the role of post-mating isolation. A geographic cline approach confirmed strong reproductive isolation and high effective selection preventing extensive introgression outside of the contact zone; and detected a signal of hybrid zone movement towards P. bocagei distribution. Genomic cline analysis revealed heterogeneous patterns of introgression among loci within the syntopy zone, but most of the loci do not introgress more or less than the genomic average maintaining a strong association with the genomic background of origin. However, genomic clines can be driven by confounding effects resulting in incongruences between both cline approaches. Importantly, overall patterns of introgression seem to result from strong intrinsic barriers across the genome, without clear “islands of differentiation”. Last, an important role of the Z chromosome in reproductive isolation is suggested.
Low vagility species may hold strong genetic signatures of past biogeographic processes but are also vulnerable to habitat loss. Flightless grasshoppers of the morabine group were once widespread in south-eastern Australia including Tasmania but are becoming restricted to remnant patches of vegetation, with local ranges impacted by agriculture and development as well as management. Habitat fragmentation can generate genetically differentiated “island” populations with low genetic variation. However, following revegetation, populations could be re-established and gene flow increased. Here we characterise SNP based genetic variation in a widespread chromosomal race of the morabine Vandiemenella viatica (race 19) to investigate the genetic health of remnant populations and to provide guidelines for restoration efforts. We update the distribution of this race to new sites in Victoria and Tasmania, and show that V. viatica populations from northern Tasmania and eastern Victoria have reduced genetic variation compared to other mainland populations. In contrast there was no effect of habitat fragment size on genetic variation. Tasmanian V. viatica populations fell into two groups, one connected genetically to eastern Victoria and the other connected to south-western Victoria. Mainland populations showed isolation by distance. These patterns are consistent with expectations from past biogeographic processes rather than local recent population fragmentation and emphasize the importance of small local reserves in preserving genetic variation. The study highlights how genomic analyses can combine information on genetic variability and population structure to identify biogeographic patterns within a species, which in turn can inform decisions on potential source populations for translocations.
Adaptation to changing environments often requires meaningful phenotypic modifications to match the current conditions. However, obtaining information about the surroundings during an organism’s own lifetime may only permit accommodating relatively late developmental modifications. Therefore, it may be advantageous to rely on inter-generational or trans-generational cues that provide information about the environment as early as possible to allow development along an optimal trajectory. Transfer of information or resources across generations, known as parental effects, is well documented in animals and plants but not in other eukaryotes, such as fungi. Understanding parental effects and their evolutionary consequences in fungi is of vital importance as they perform crucial ecosystem functions. In this study, we investigated whether parental effects are present in the filamentous fungus Neurospora crassa, how long do they last, are the effects adaptive, and what is their mechanism. We performed a fully factorial match / mismatch experiment for a good and poor quality environment, in which we measured mycelium size of strains that experienced either a matched or mismatched environment in their previous generation. We found a strong silver spoon effect in initial mycelium growth, which lasted for one generation, and increased fitness during competition experiments. By using deletion mutants that lacked key genes in epigenetic processes, we show that epigenetic mechanisms are not involved in this effect. Instead, we show that spore glycogen content, glucose availability and a radical transcription shift in spores are the main mechanisms behind this parental effect.
Divergence in the face of high dispersal capabilities is a documented but poorly understood phenomenon. The white-tailed eagle (Haliaeetus albicilla) has a large geographic dispersal capability and should theoretically be able to maintain genetic homogeneity across its dispersal range. However, following analysis of the genomic variation of white-tailed eagles, from both historical and contemporary samples, clear signatures of ancient biogeographic substructure across Europe and the North-East Atlantic is observed. The greatest genomic differentiation was observed between island (Greenland and Iceland) and mainland (Denmark, Norway and Estonia) populations. The two island populations share a common ancestry from a single mainland population, distinct from the other sampled mainland populations, and despite the potential for high connectivity between Iceland and Greenland they are well separated from each other and are characterized by inbreeding and little variation. Temporal differences also highlight a pattern of regional populations persisting despite the potential for admixture. All sampled populations generally showed a decline in effective population size over time, which may have been shaped by four historical events: I) isolation of refugia during the last glacial period 110-115,000 years ago, II) population divergence following the colonization of the deglaciated areas ~10,000 years ago, III) human population expansion, which led to the settlement in Iceland ~1,100 years ago, and IV) human persecution and exposure to toxic pollutants during the last two centuries.
Indirect genetic effects describe phenotypic variation that results from differences in the genotypic composition of social partners. Such effects represent heritable sources of environmental variation in eusocial organisms because individuals are typically reared by their siblings. In the fire ant Solenopsis invicta, a social supergene exhibits striking indirect genetic effects on worker regulation of colony queen number, such that the genotypic composition of workers at the supergene determines whether colonies contain a single or multiple queens. We assessed the direct and indirect genetic effects of this supergene on gene expression in brains and abdominal tissues from lab-reared workers and compared these with previously published data from field-collected pre-reproductive queens. We found that direct genetic effects caused larger gene expression changes and were more consistent across tissue types and castes than indirect genetic effects. Indirect genetic effects influenced the expression of many loci but were generally restricted to the abdominal tissues. Further, indirect genetic effects were only detected when the genotypic composition of social partners differed throughout the development and adult life of focal workers, and were often only significant with relatively lenient statistical cutoffs. Our study provides insight into direct and indirect genetic effects of a social supergene on gene regulatory dynamics across tissues and castes in a complex society.
In free-living ecological communities, organismal life histories shape interactions with their environment, which ultimately forms the basis of ecological succession. Individual animals in natural populations tend to host diverse parasite species concurrently over their lifetimes. However, the structure and dynamics of mammalian parasite communities have not been contextualized in terms of primary ecological succession, in part because few datasets track occupancy and abundance of multiple parasites in wild hosts starting at birth. Here, we studied community dynamics of twelve subtypes of protozoan microparasites (Theileria spp.) in a herd of African buffalo. We show that Theileria communities followed predictable patterns of succession underpinned by four different parasite life-history strategies. In contrast to many free-living communities, network complexity decreased with host age. Examining parasite communities through the lens of succession may better inform the effect of complex within host eco-evolutionary dynamics on infection outcomes, including parasite co-existence through the lifetime of the host.
Adaptive phenotypes are shaped by a combination of genetic and environmental forces, and while the literature is rich with studies focusing on either genetics or environment contributions, those that consider both are rare. Here we utilize the cichlid oral jaw apparatus to fill this knowledge-gap. First, we employed RNA-seq in bony and ligamentous tissues important for jaw opening to identify differentially expressed genes between species and across foraging environments. Our foraging treatments were designed to force animals to employ either suction or biting/scraping, which broadly mimic pelagic or benthic modes of feeding. We found a large number of differentially expressed genes between species, and while we identified relatively few differences between environments, species differences were far more pronounced when reared in the pelagic versus benthic environment. Further, these data carried the signature of genetic assimilation, and implicated cell cycle regulation in shaping the jaw across species and environments. Next, we repeated the foraging experiment and performed ATAC-seq procedures on nuclei harvested from the same tissues. Cross-referencing results from both analyses revealed subsets of genes that were both differentially expressed and differentially accessible in either the pelagic (n=15) or the benthic environment (n=11), as well as loci where differences were robust to foraging environment (n=13). All in all, these data provide novel insights into the epigenetic, genetic, and cellular bases of species- and environment-specific bone shapes, as well as the evolution of phenotypic plasticity in this iconic model system.
Linear infrastructure stands as one of the main culprits of anthropogenically caused biodiversity decline. As it fragments landscapes, it ultimately results in a myriad of direct and indirect ecological consequences for wildlife. As transportation networks will continue to grow under increasing human population growth, biodiversity will continue to decline making the need to understand and mitigate their impact on species an urgent need for conservation worldwide. The implementation of mitigation measures to alleviate the barrier effect produced by linear transport infrastructure on local fauna is not new, and research has shown that their effectiveness has been shown to be influenced by their design, their placement and the biology of the impacted species. Our understanding of their effectiveness in preventing the longer-term impacts of linear transport infrastructure on habitat connectivity via gene flow, however, remains poorly understood. Here, we used a pre- and post-habitat fragmentation genetic dataset collected as part of an extensive Koala Management Program to ask questions about the immediate and predicted longer-term genetic consequences of linear transport infrastructure on the impacted species. Importantly, using forward migration simulations, we show that to preserve connectivity would need to result in around 20% of the population mixing to avoid long-term genetic drift. These results have important consequences for the management of species at the forefront of linear infrastructure. In particular, the study shows the importance of considering gene flow in our assessment of the effectiveness of fauna crossings.
By evaluating genetic variation across the entire genome, one can address existing questions in a novel way while new can be asked. Such questions include how different local environments influence both adaptive and neutral genomic variation within and among populations, providing insights not only into local adaptation of natural populations, but also into their responses to global change and the exploitation-induced evolution. Here, under a seascape genomic approach, ddRAD genomic data were used along with environmental information to uncover the underlying processes (migration, selection) shaping European sardines (Sardina pilchardus) of the Western Mediterranean and adjacent Atlantic waters. This information can be relevant to the (re)definition of fishery stocks, and their short-term adaptive potential. We found that studied sardine samples form two clusters, detected using both neutral and adaptive (outlier) loci suggesting that natural selection and local adaptation play a key role in driving genetic change among the Atlantic and the Mediterranean sardines. Temperature and especially the trend in the number of days with sea surface temperature (SST) above 19oC was crucial at all levels of population structuring with implications on species’ key biological processes, especially reproduction. Our findings provide evidence for a dynamic equilibrium where population structure is maintained by physical and biological factors under the opposing influences of migration and selection. Given its dynamic nature, such a system postulates a continuous monitoring under a seascape genomic approach that can benefit by incorporating a temporal as well as a more detailed spatial dimension.
Anthropogenic biological invasions represent major concerns but enable us to investigate rapid evolutionary changes and adaptation to novel environments. The goldfish Carassius auratus with sexual diploids and asexual triploids coexisting in natural waters, is one of the most widespread invasive fishes in Tibet, providing an ideal model to study evolutionary processes during invasion in different reproductive forms from the same vertebrate. Here, using whole-genome resequencing data of 151 C. auratus individuals from invasive and native ranges, we found different patterns of genomic responses between diploid and triploid populations during their invasion to Tibet. For diploids, although invasive individuals derived from two different genetically distinct sources and had a relative higher diversity (π) at the population level, their individual genetic diversity (genome-wide observed heterozygosity) was significantly lower (21.4%) than that of source individuals. Population structure analysis revealed that the invasive individuals formed a specific genetic cluster distinct from the source populations. Runs of homozygosity analysis showed low inbreeding only in invasive individuals, and only the invasive population experienced a recent decline in effective population size reflecting founder events. For triploids, however, invasive populations showed no loss of individual genetic diversity and no genetic differentiation relative to source populations. Regions of putative selective sweeps between invasive and source populations of diploids mainly involved genes associated with mannosidase activity and embryo development. Our results suggest invasive diploids deriving from distinct sources still lost individual genetic diversity resulting from recent inbreeding and founder events and selective sweeps, and invasive triploids experienced no genetic change owing to their reproduction mode of gynogenesis that precludes inbreeding and founder effects and may make them more powerful invaders.
Pregnancy, the post-fertilization period when embryos are incubated within the body, is a dynamic multistage process that has convergently evolved in many vertebrates. To increase independence from environmental fluctuations and protect offspring from predation, challenges had to be initially overcome. The most obvious, when considering such an intimate relation between the parent and its semi-allogenic offspring, was the pressing need to dodge immunity-associated embryo rejection. In mammals, immunological tolerance was found to be dependent on the active modulation of the immune system. Even though supporting much of the current knowledge on vertebrate pregnancy, mammals lack extant transitional stages that could help reconstruct the evolutionary pathway of this fascinatingly complex reproduction mode. In this issue of Molecular Ecology, Parker et al. (2022) selected an untraditional model - the seahorse and pipefish family, whose species evolved male pregnancy across an almost continuous gradient of complexity, from external oviparity to internal gestation. By contrasting gene expression profiles of syngnathids with distinct brooding architectures, this study allowed for the observation of subtle evolutionary adaptations, while confirming the existence of remarkable similarities to ‘female’ pregnancy (e.g., the evolution of male pregnancy in pouched species occurred alongside immune downregulation, and inflammation seems vital during early pregnancy stages). In a world where the debate on sex-roles takes centre stage, Parker et al. (2022) appeasing results hint at the fact that the strongly convergent evolution of vertebrate pregnancy was seemingly unaffected by which sex carries the burden of gestation.