Sandrine Sauzet

Structural and Functional Evolution of the Pineal Melatonin System in Vertebrates

In most species daily rhythms are synchronized by the photoperiodic cycle. They are generated by the circadian system, which is made of a pacemaker, an entrainment pathway to this clock, and one or more output signals. In vertebrates, melatonin produced by the pineal organ is one of these outputs. The production of this time‐keeping hormone is high at night and low during the day. Despite the fact that this is a well‐preserved pattern, the pathways through which the photoperiodic information controls the rhythm have been profoundly modified from early vertebrates to mammals. The photoperiodic control is direct in fish and frogs and indirect in mammals. In the former, full circadian systems are found in photoreceptor cells of the pineal organ, retina, and possibly brain, thus forming a network where melatonin could be a hormonal synchronizer. In the latter, the three elements of a circadian system are scattered: the photoreceptive units are in the eyes, the clocks are in the suprachiasmatic nuclei of the hypothalamus, and the melatonin‐producing units are in the pineal cells. Intermediate situations are observed in sauropsids. Differences are also seen at the level of the arylalkylamine N‐acetyltransferase (AANAT), the enzyme responsible for the daily variations in melatonin production. In contrast to tetrapods, teleost fish AANATs are duplicated and display tissue‐specific expression; also, pineal AANAT is special—it responds to temperature in a species‐specific manner, which reflects the fish ecophysiological preferences. This review summarizes anatomical, structural, and molecular aspects of the evolution of the melatonin‐producing system in vertebrates.

Drastic neofunctionalization associated with evolution of the timezyme AANAT 500 Mya

Significance The pineal gland is dedicated to the production of melatonin. Submammalian pineal glands can also detect light, and the retinas of many species can make melatonin. From this finding and others, it is seems that both tissues evolved from a common ancestral photodetector. A key factor driving their independent evolution may have been the evolution of melatonin synthesis and more specifically, the timezyme, a form of arylalkylamine N-acetyltransferase (AANAT) that plays a key role in controlling rhythmic production of melatonin. The current report indicates that the timezyme evolved from a primitive form of AANAT over 500 Mya in chordate evolution through a process of gene duplication followed by rapid neofunctionalization and that it was not a posthoc acquisition. Melatonin (N-acetyl-5-methoxytrypamine) is the vertebrate hormone of the night: circulating levels at night are markedly higher than day levels. This increase is driven by precisely regulated increases in acetylation of serotonin in the pineal gland by arylalkylamine N-acetyltransferase (AANAT), the penultimate enzyme in the synthesis of melatonin. This unique essential role of AANAT in vertebrate timekeeping is recognized by the moniker the timezyme. AANAT is also found in the retina, where melatonin is thought to play a paracrine role. Here, we focused on the evolution of AANAT in early vertebrates. AANATs from Agnathans (lamprey) and Chondrichthyes (catshark and elephant shark) were cloned, and it was found that pineal glands and retinas from these groups express a form of AANAT that is compositionally, biochemically, and kinetically similar to AANATs found in bony vertebrates (VT-AANAT). Examination of the available genomes indicates that VT-AANAT is absent from other forms of life, including the Cephalochordate amphioxus. Phylogenetic analysis and evolutionary rate estimation indicate that VT-AANAT evolved from the nonvertebrate form of AANAT after the Cephalochordate–Vertebrate split over one-half billion years ago. The emergence of VT-AANAT apparently involved a dramatic acceleration of evolution that accompanied neofunctionalization after a duplication of the nonvertebrate AANAT gene. This scenario is consistent with the hypotheses that the advent of VT-AANAT contributed to the evolution of the pineal gland and lateral eyes from a common ancestral photodetector and that it was not a posthoc recruitment.

Fruiting Strategies of Perennial Plants: A Resource Budget Model to Couple Mast Seeding to Pollination Efficiency and Resource Allocation Strategies

Masting, a breeding strategy common in perennial plants, is defined by seed production that is highly variable over years and synchronized at the population level. Resource budget models (RBMs) proposed that masting relies on two processes: (i) the depletion of plant reserves following high fruiting levels, which leads to marked temporal fluctuations in fruiting; and (ii) outcross pollination that synchronizes seed crops among neighboring trees. We revisited the RBM approach to examine the extent to which masting could be impacted by the degree of pollination efficiency, by taking into account various logistic relationships between pollination success and pollen availability. To link masting to other reproductive traits, we split the reserve depletion coefficient into three biological parameters related to resource allocation strategies for flowering and fruiting. While outcross pollination is considered to be the key mechanism that synchronizes fruiting in RBMs, our model counterintuitively showed that intense masting should arise under low-efficiency pollination. When pollination is very efficient, medium-level masting may occur, provided that the costs of female flowering (relative to pollen production) and of fruiting (maximum fruit set and fruit size) are both very high. Our work highlights the powerful framework of RBMs, which include explicit biological parameters, to link fruiting dynamics to various reproductive traits and to provide new insights into the reproductive strategies of perennial plants.

Somatotropic axis genes are expressed before pituitary onset during zebrafish and sea bass development.

The somatotropic axis, or growth hormone-insulin-like growth factor-1 (GH-IGF-1) axis, of fish is involved in numerous physiological process including regulation of ionic and osmotic balance, lipid, carbohydrate and protein metabolism, growth, reproduction, immune function and behavior. It is thought that GH plays a role in fish development but conflicting results have been obtained concerning the ontogeny of the somatotropic axis. Here we investigated the developmental expression of GH, GH-receptor (GHR) and IGF-1 genes and of a GH-like protein from fertilization until early stages of larval development in two Teleosts species, Danio rerio and Dicentrarchus labrax, by PCR, in situ hybridization and Western blotting. GH, GHR and IGF-1 mRNA were present in unfertilized eggs and at all stages of embryonic development, all three displaying a similar distribution in the two species. First located in the whole embryo (until 12 hpf in zebrafish and 76 hpf in sea bass), the mRNAs appeared then distributed in the head and tail, from where they disappeared progressively to concentrate in the forming pituitary gland. Proteins immunoreactive with a specific sea bass anti-GH antibody were also detected at all stages in this species. Differences in intensity and number of bands suggest that protein processing varies from early to later stages of development. The data show that all actors of the somatotropic axis are present from fertilization in these two species, suggesting they plays a role in early development, perhaps in an autocrine/paracrine mode as all three elements displayed a similar distribution at each stage investigated.

Cognitive adaptation in asexual and sexual wasps living in contrasted environments

Differences in learning and memory dynamics between populations are suspected to result from differences in ecological constraints such as resource distribution. The two reproductive modes (strains) of the parasitoid wasp Venturia canescens share the same geographical areas but live in contrasting habitats: arrhenotokous wasps live in the wild (generally orchards), whereas thelytokous ones live mostly in stored-products buildings (e.g. granaries). This species thus represents a relevant biological model for understanding the relationship between the ecological constraints faced by a species and its memory and learning ability. We showed that after having laid eggs in presence of both a synthetic odour and natural olfactory cues of their host, arrhenotokous wasps exhibited a change in their behavioural response towards the synthetic odour that was at least as pronounced as in thelytokous ones even though they were faster in their decision-making process. This is consistent with better learning skills in arrhenotokous wasps. The corresponding memory trace persisted in both strains for at least 51 h. We compare and discuss the learning and memory ablities of both strains as a function of their costs and benefits in their preferential habitats.

Faithful or not: direct and indirect effects of climate on extra-pair paternities in a population of Alpine marmots.

Despite being identified an area that is poorly understood regarding the effects of climate change, behavioural responses to climatic variability are seldom explored. Climatic variability is likely to cause large inter-annual variation in the frequency of extra-pair litters produced, a widespread alternative mating tactic to help prevent, correct or minimize the negative consequences of sub-optimal mate choice. In this study, we investigated how climatic variability affects the inter-annual variation in the proportion of extra-pair litters in a wild population of Alpine marmots. During 22 years of monitoring, the annual proportion of extra-pair litters directly increased with the onset of earlier springs and indirectly with increased snow in winters. Snowier winters resulted in a higher proportion of families with sexually mature male subordinates and thus, created a social context within which extra-pair paternity was favoured. Earlier spring snowmelt could create this pattern by relaxing energetic, movement and time constraints. Further, deeper snow in winter could also contribute by increasing litter size and juvenile survival. Optimal mate choice is particularly relevant to generate adaptive genetic diversity. Understanding the influence of environmental conditions and the capacity of the individuals to cope with them is crucial within the context of rapid climate change.

Insects and incest: sib-mating tolerance in natural populations of a parasitoid wasp

Sib-mating avoidance is a pervasive behaviour that likely evolves in species subject to inbreeding depression. Laboratory studies have provided elegant demonstrations of sib-mating avoidance, but small-scale bioassays often minimize the costs associated with mate finding and choice, which could lead to spurious findings. We used the hymenopteran parasitoid wasp Venturia canescens as a model organism, because previous laboratory studies revealed that sib-mating led to a 25% decrease in fertile offspring, and that sib-mating was partially avoided. Our study consisted of a mate choice experiment in laboratory cages to determine if kin discrimination occurs in this species. We further performed a field study in which 86 wild-caught males, 155 wild-caught females and their 226 daughters daughters were genotyped at eighteen microsatellite loci. With these field data, we reconstructed the genotype of each female’s mate and estimated the relatedness of each mating pair. Mate choice experiments confirmed that females are capable of discriminating kin. Time to mating depended on the frequency of female encounters with related and unrelated males. Contrary to previously published results, however, no sib-mating avoidance was detected. In the field, the effective rate of sib-mating did not differ from the probability that sibs encounter one other at random, which corroborates the absence of sib-mating avoidance. We also detected a weak but significant male bias in dispersal, which could reduce encounters between sibs. Our results suggest that, despite kin discrimination, V. canescens tolerates sib-mating in the field. The weak male-biased dispersal cannot explain entirely this pattern. This raises the question as to why kin discrimination is maintained in this species. It further calls into question the idea that inbreeding depression occurs in most species with single-locus complementary sex determination.Sib mating avoidance is a pervasive behaviour, which likely evolves in species that sare subject to inbreeding depression. Laboratory studies have provided elegant demonstrations, but small-scale bioassays often minimize the costs associated with mate finding and mate-choice and may for this reason produce spurious findings. We inferred the mating behaviour of the parasitoid wasp Venturia canescens from the genetic analyses of natural populations. We used V. canescens as a model organism because in this species, laboratory experiments have shown that sib mating yields a 25% decrease in fertile offspring, and congruently, sib mating is partially avoided. Our study consisted in genotyping 86 wild-caught males, 155 wild-caught-females and their 226 daughters at eighteen microsatellite loci. With these data, we were able to reconstruct the genotype of females9 mate and estimate the relatedness of each mating pairs. We found that the effective rate of sib mating does not differ from the probability that sibs encounter one another at random, which suggest a sib mating tolerance in this species. However, complementary lab experiments confirmed that kin discrimination exist in this species, with related pairs having a lower mating latency. These results suggest that V. canescens tolerate sib mating in the field despite kin discrimination, and therefore call into question the common beliefs on inbreeding depression in species with single-locus complementary sex determination. This inbreeding tolerance also opens up the question of the maintenance of the kin discrimination in this species.