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

Marine 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 remain largely unknown. Additionally, many populations have declined drastically 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 green (Chelonia mydas) and leatherback (Dermochelys coriacea) turtles, representing the two extant marine turtle families (MRCA ~60 MYA). Generally, these genomes are highly syntenic and homologous. Non-collinearity was associated with higher copy numbers of immune, zinc-finger, or olfactory receptor (OR) genes in green turtles. Gene family analyses suggested that ORs related to waterborne odorants have expanded in green turtles and contracted in leatherbacks, which may underlie immunological and sensory adaptations assisting navigation and occupancy of neritic versus pelagic environments, and diet specialization. Microchromosomes showed reduced collinearity, and greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, demographic history and diversity analyses showed stark contrasts between species, indicating that leatherback turtles have had a low yet stable effective population size, extremely low diversity when compared to other reptiles, and a higher proportion of deleterious variants, reinforcing concern over the persistence of this species under future climate scenarios. These highly contiguous genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.

Temporal niche partitioning as a novel mechanism promoting co-existence of sympatric predators in marine systems

Niche partitioning of time, space or resources is considered the key to allowing the coexistence of competitor species, and particularly guilds of predators. However, the extent to which these processes occur in marine systems is poorly understood due to the difficulty in studying fine-scale movements and activity patterns in mobile underwater species. Here, we used acceleration data-loggers to investigate temporal partitioning in a guild of marine predators. Six species of co-occurring large coastal sharks demonstrated distinct diel patterns of activity, providing evidence of strong temporal partitioning of foraging times. This is the first instance of diel temporal niche partitioning described in a marine predator guild, and is probably driven by a combination of physiological constraints in diel timing of activity (e.g. sensory adaptations) and interference competition (hierarchical predation within the guild), which may force less dominant predators to suboptimal foraging times to avoid agonistic interactions. Temporal partitioning is often thought to be rare compared to other partitioning mechanisms, but the occurrence of temporal partitioning here and similar characteristics in many other marine ecosystems (multiple predators simultaneously present in the same space with dietary overlap) introduces the question of whether this is a common mechanism of resource division in marine systems.

Sensory adaptations reshaped intrinsic factors underlying morphological diversification in bats

Background Morphological evolution may be impacted by both intrinsic (developmental, constructional, physiological) and extrinsic (ecological opportunity and release) factors, but can intrinsic factors be altered by adaptive evolution and, if so, do they constrain or facilitate the subsequent diversification of biological form? Bats underwent deep adaptive divergences in skull shape as they evolved different sensory modes; here we investigate the potential impact of this process on two intrinsic factors that underlie morphological variation across organisms, allometry, and modularity. Results We use comparative phylogenetic and morphometric approaches to examine patterns of evolutionary allometry and modularity across a 3D geometric morphometric dataset spanning all major bat clades. We show that allometric relationships diverge between echolocators and visually oriented non-echolocators and that the evolution of nasal echolocation reshaped the modularity of the bat cranium. Conclusions Shifts in allometry and modularity may have significant consequences on the diversification of anatomical structures, as observed in the bat skull.

Dopamine Modulation of Motor and Sensory Cortical Plasticity among Vertebrates

Synopsis Goal-directed learning is a key contributor to evolutionary fitness in animals. The neural mechanisms that mediate learning often involve the neuromodulator dopamine. In higher order cortical regions, most of what is known about dopamine’s role is derived from brain regions involved in motivation and decision-making, while significantly less is known about dopamine’s potential role in motor and/or sensory brain regions to guide performance. Research on rodents and primates represents over 95% of publications in the field, while little beyond basic anatomy is known in other vertebrate groups. This significantly limits our general understanding of how dopamine signaling systems have evolved as organisms adapt to their environments. This review takes a pan-vertebrate view of the literature on the role of dopamine in motor/sensory cortical regions, highlighting, when available, research on non-mammalian vertebrates. We provide a broad perspective on dopamine function and emphasize that dopamine-induced plasticity mechanisms are widespread across all cortical systems and associated with motor and sensory adaptations. The available evidence illustrates that there is a strong anatomical basis—dopamine fibers and receptor distributions—to hypothesize that pallial dopamine effects are widespread among vertebrates. Continued research progress in non-mammalian species will be crucial to further our understanding of how the dopamine system evolved to shape the diverse array of brain structures and behaviors among the vertebrate lineage.

Behavioral and genomic sensory adaptations underlying the pest activity of Drosophila suzukii

Studying how novel phenotypes originate and evolve is fundamental to the field of evolutionary biology as it allows us to understand how organismal diversity is generated and maintained. However, determining the basis of novel phenotypes is challenging as it involves orchestrated changes at multiple biological levels. Here, we aim to overcome this challenge by using a comparative species framework combining behavioral, gene expression, and genomic analyses to understand the evolutionary novel egg-laying substrate-choice behavior of the invasive pest species Drosophila suzukii. First, we used egg-laying behavioral assays to understand the evolution of ripe fruit oviposition preference in D. suzukii as compared to closely related species D. subpulchrella and D. biarmipes, as well as D. melanogaster. We show that D. subpulchrella and D. biarmipes lay eggs on both ripe and rotten fruits, suggesting that the transition to ripe fruit preference was gradual. Secondly, using two-choice oviposition assays, we studied how D. suzukii, D. subpulchrella, D. biarmipes and D. melanogaster differentially process key sensory cues distinguishing ripe from rotten fruit during egg-laying. We found that D. suzukii’s preference for ripe fruit is in part mediated through a species-specific preference for stiff substrates. Lastly, we sequenced and annotated a high-quality genome for D. subpulchrella. Using comparative genomic approaches, we identified candidate genes involved in D. suzukii’s ability to seek out and target ripe fruits. Our results provide detail to the stepwise evolution of pest activity in D. suzukii, indicating important cues used by this species when finding a host, and the molecular mechanisms potentially underlying their adaptation to a new ecological niche.

Differential investment in visual and olfactory brain regions mirrors the sensory needs of a paper wasp social parasite and its host

ABSTRACTObligate social parasites evolve traits to effectively locate and then exploit their hosts, whereas hosts have complex social behavioral repertoires, which include sensory recognition to reject potential conspecific intruders and heterospecific parasites. While social parasite and host behaviors have been studied extensively, less is known about how their sensory systems function to meet their specific selective pressures. Here, we compare investment in visual and olfactory brain regions in the paper wasp Polistes dominula, and its obligate social parasite P. sulcifer, to explore the link between sensory systems and brain plasticity. Our results show opposite and significant differences, consistent with their very different life-histories, in the sensory investments between these two closely-related species. Social parasites initially invest in the optic lobes to likely locate their hosts. After host colony usurpation, the parasite increases its brain volume, with specific investment in antennal lobes, which mirrors the behavioral switch from a usurping parasite to an integrated parasitic queen of the host colony. Contrastingly, hosts initially invest in the antennal lobes and sensory processing compared to social parasites, as predicted by their need to maintain social cohesion, allocate colony tasks, and recognize con- and heterospecific intruders. Host queens show a trend of higher investment in all sensory brain regions compared to workers, paralleling differences in task allocations. Our work provides novel insights into how intraspecific brain plasticity can facilitate the unique sensory adaptations needed to perform specific tasks by the host or to transition from searching to successful host exploitation by the social parasite.

Echolocating bats can adjust sensory acquisition based on internal cues

Background Sensory systems acquire both external and internal information to guide behavior. Adjustments based on external input are much better documented and understood than internal-based sensory adaptations. When external input is not available, idiothetic—internal—cues become crucial for guiding behavior. Here, we take advantage of the rapid sensory adjustments exhibited by bats in order to study how animals rely on internal cues in the absence of external input. Constant frequency echolocating bats are renowned for their Doppler shift compensation response used to adjust their emission frequency in order to optimize sensing. Previous studies documented the importance of external echoes for this response. Results We show that the Doppler compensation system works even without external feedback. Bats experiencing accelerations in an echo-free environment exhibited an intact compensation response. Moreover, using on-board GPS tags on free-flying bats in the wild, we demonstrate that the ability to perform Doppler shift compensation response based on internal cues might be essential in real-life when echo feedback is not available. Conclusions We thus show an ecological need for using internal cues as well as an ability to do so. Our results illustrate the robustness of one particular sensory behavior; however, we suggest this ability to rely on different streams of information (i.e., internal or external) is probably relevant for many sensory behaviors.

Behavioral and genomic sensory adaptations underlying the pest activity of Drosophila suzukii

ABSTRACTStudying how novel phenotypes originate and evolve is fundamental to the field of evolutionary biology as it allows us to understand how organismal diversity is generated and maintained. However, determining the basis of novel phenotypes is challenging as it involves orchestrated changes at multiple biological levels. Here, we aim to overcome this challenge by using a comparative species framework combining behavioral, gene expression, and genomic analyses to understand the evolutionary novel egg-laying substrate-choice behavior of the invasive pest species Drosophila suzukii. First, we used egg-laying behavioral assays to understand the evolution of ripe fruit oviposition preference in D. suzukii as compared to closely related species D. subpulchrella and D. biarmipes, as well as D. melanogaster. We show that D. subpulchrella and D. biarmipes lay eggs on both ripe and rotten fruits, suggesting that the transition to ripe fruit preference was gradual. Secondly, using two-choice oviposition assays, we studied how D. suzukii, D. subpulchrella, D. biarmipes and D. melanogaster differentially process key sensory cues distinguishing ripe from rotten fruit during egg-laying. We found that D. suzukii’s preference for ripe fruit is in part mediated through a species-specific preference for stiff substrates. Lastly, we sequenced and annotated a high-quality genome for D. subpulchrella. Using comparative genomic approaches, we identified candidate genes involved in D. suzukii’s ability to seek out and target ripe fruits. Our results provide detail to the stepwise evolution of pest activity in D. suzukii, indicating important cues used by this species when finding a host, and the molecular mechanisms potentially underlying their adaptation to a new ecological niche.