Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals.

Molluscs have undergone many transitions between separate sexes and hermaphroditism, which is of interest in studying the evolution of sex determination and differentiation. Here, we combined multi-locus genotypes obtained from restriction site-associated DNA (RAD) sequencing with anatomical observations of the gonads of three deep-sea hydrothermal vent gastropods of the genus Alviniconcha living in the southwest Pacific. We found that all three species (Alviniconcha boucheti, Alviniconcha strummeri, and Alviniconcha kojimai) share the same male-heterogametic XY sex-determination system but that the gonads of XX A. kojimai individuals are invaded by a variable proportion of male reproductive tissue. The identification of Y-specific RAD loci (found only in A. boucheti) and the phylogenetic analysis of three sex-linked loci shared by all species suggested that X-Y recombination has evolved differently within each species. This situation of three species showing variation in gonadal development around a common sex-determination system provides new insights into the reproductive mode of poorly known deep-sea species and opens up an opportunity to study the evolution of recombination suppression on sex chromosomes and its association with mixed or transitory sexual systems.

Inter-Specific Genetic Exchange Despite Strong Divergence in Deep-Sea Hydrothermal Vent Gastropods of the Genus Alviniconcha.

Deep hydrothermal vents are highly fragmented and unstable habitats at all temporal and spatial scales. Such environmental dynamics likely play a non-negligible role in speciation. Little is, however, known about the evolutionary processes that drive population-level differentiation and vent species isolation and, more specifically, how geography and habitat specialisation interplay in the species history of divergence. In this study, the species range and divergence of Alviniconcha snails that occupy active Western Pacific vent fields was assessed by using sequence variation data of the mitochondrial Cox1 gene, RNAseq, and ddRAD-seq. Combining morphological description and sequence datasets of the three species across five basins, we confirmed that A. kojimai, A. boucheti, and A. strummeri, while partially overlapping over their range, display high levels of divergence in the three genomic compartments analysed that usually encompass values retrieved for reproductively isolated species with divergences rang from 9% to 12.5% (mtDNA) and from 2% to 3.1% (nuDNA). Moreover, the three species can be distinguished on the basis of their external morphology by observing the distribution of bristles and the shape of the columella. According to this sampling, A. boucheti and A. kojimai form an east-to-west species abundance gradient, whereas A. strummeri is restricted to the Futuna Arc/Lau and North Fiji Basins. Surprisingly, population models with both gene flow and population size heterogeneities among genomes indicated that these three species are still able to exchange genes due to secondary contacts at some localities after a long period of isolation.

Subtle limits to connectivity revealed by outlier loci within two divergent metapopulations of the deep-sea hydrothermal gastropod Ifremeria nautilei.

Hydrothermal vents form archipelagos of ephemeral deep-sea habitats that raise interesting questions about the evolution and dynamics of the associated endemic fauna, constantly subject to extinction-recolonization processes. These metal-rich environments are coveted for the mineral resources they harbour, thus raising recent conservation concerns. The evolutionary fate and demographic resilience of hydrothermal species strongly depend on the degree of connectivity among and within their fragmented metapopulations. In the deep sea, however, assessing connectivity is difficult and usually requires indirect genetic approaches. Improved detection of fine-scale genetic connectivity is now possible based on genome-wide screening for genetic differentiation. Here, we explored population connectivity in the hydrothermal vent snail Ifremeria nautilei across its species range encompassing five distinct back-arc basins in the Southwest Pacific. The global analysis, based on 10,570 single nucleotide polymorphism (SNP) markers derived from double digest restriction-site associated DNA sequencing (ddRAD-seq), depicted two semi-isolated and homogeneous genetic clusters. Demogenetic modeling suggests that these two groups began to diverge about 70,000 generations ago, but continue to exhibit weak and slightly asymmetrical gene flow. Furthermore, a careful analysis of outlier loci showed subtle limitations to connectivity between neighbouring basins within both groups. This finding indicates that migration is not strong enough to totally counterbalance drift or local selection, hence questioning the potential for demographic resilience at this latter geographical scale. These results illustrate the potential of large genomic data sets to understand fine-scale connectivity patterns in hydrothermal vents and the deep sea.

Antarctic krill (Euphausia superba) in a warming ocean: thermotolerance and deciphering Hsp70 responses.

The Antarctic krill, Euphausia superba, is a Southern Ocean endemic species of proven ecological importance to the region. In the context of predicted global warming, it is particularly important to understand how classic biomarkers of heat stress function in this species. In this respect, Hsp70s are acknowledged as good candidates. However, previous studies of expression kinetics have not been able to demonstrate significant upregulation of these genes in response to heat shocks at 3 °C and 6 °C for 3 and 6 h. The current work complements these previous results and broadens the prospects for the use of Hsp70s as a relevant marker of thermal shock in this krill species. New experiments demonstrate that induction of Hsp70 isoforms was not detected during exposure to heat shock, but increased expression was observed after several hours of recovery. To complete the analysis of the expression kinetics of the different isoforms, experiments were carried out over short time scales (1 and 2 h at 3 °C and 6 °C) as well as at higher temperatures (9 °C, 12 °C, and 15 °C for 3 h), without any significant response. A 6-week monitoring of animals at 3 °C showed that the time factor is decisive in the establishment of the response. CTmax experiments with incremental times of 1 °C per day or 1 °C every 3 days have shown a particularly high resilience of the animals. The demonstration of the abundance of Hsp70s present before thermal stress in various species of krill, as well as in specimens of E. superba of various origins, showed that the delay in the response in expression could be related to the high constitutive levels of Hsp70 available before the stress experiments. The alternative labelling of the two main isoforms of Hsp70 according to the origin of the animals allowed hypotheses to be put forward on the functioning of thermoregulation in Antarctic krill as well as ice krill.

Young parents produce offspring with short telomeres: A study in a long-lived bird, the Black-browed Albatross (Thalassarche melanophrys).

In wild vertebrates, young parents are less likely to successfully rear offspring relative to older ones because of lower parental skills ('the constraint hypothesis'), lower parental investment ('the restraint hypothesis') or because of a progressive disappearance of lower-quality individuals at young ages ('the selection hypothesis'). Because it is practically difficult to follow an offspring during its entire life, most studies have only focused on the ability of individuals to breed or produce young, while neglecting the ability of such young to subsequently survive and reproduce. Several proxies of individual quality can be useful to assess the ability of young to survive and recruit into the population. Among them, telomere length measurement appears especially promising because telomere length has been linked to longevity and fitness in captive and wild animals. By sampling 51 chicks reared by known-aged parents, we specifically tested whether parental age was correlated to offspring telomere length and body condition in a long-lived bird species, the Black-browed Albatross (Thalassarche melanophrys). Young Black-browed albatrosses produced chicks with shorter telomere relative to those raised by older ones. Short offspring telomeres could result from poor developmental conditions or heritability of telomere length. Moreover, young parents also had chicks of lower body condition when compared with older parents, although this effect was significant in female offspring only. Overall, our study demonstrates that parental age is correlated to two proxies of offspring fitness (body condition and telomere length), suggesting therefore that older individuals provide better parental cares to their offspring because of increased parental investment (restraint hypothesis), better foraging/parental skills (constraint hypothesis) or because only high-quality individuals reach older ages (selection hypothesis).

Shorter telomeres precede population extinction in wild lizards.

Identifying the early warning signals of catastrophic extinctions has recently become a central focus for ecologists, but species' functional responses to environmental changes remain an untapped source for the sharpening of such warning signals. Telomere length (TL) analysis represents a promising molecular tool with which to raise the alarm regarding early population decline, since telomere attrition is associated with aging processes and accelerates after a recurrent exposure to environmental stressors. In the southern margin of their range, populations of the common lizard (Zootoca vivipara) recently became extinct at lowest elevations due to changes in climate conditions. However, the proximal signals involved in these demographic declines are still unknown. Here, we sampled 100 yearling lizards from 10 natural populations (n = 10 per population) along an extinction risk gradient. Relative lizard abundance dramatically dropped over 12 years in low-altitude populations characterized by warmer ambient temperatures and higher body growth of lizards early in life. A non-linear relationship was found between TL and population extinction risk, with shorter telomeres in populations facing high risk of extinction when compared to non-threatened ones. Our results identify TL as a promising biomarker and imply that population extinctions might be preceded by a loop of physiological aging.

Exposure to oxychlordane is associated with shorter telomeres in arctic breeding kittiwakes.

Telomeres are DNA-protein complexes located at the end of chromosomes, which play an important role in maintaining the genomic integrity. Telomeres shorten at each cell division and previous studies have shown that telomere length is related to health and lifespan and can be affected by a wide range of environmental factors. Among them, some persistent organic pollutants (POPs) have the potential to damage DNA. However, the effect of POPs on telomeres is poorly known for wildlife. Here, we investigated the relationships between some legacy POPs (organochlorine pesticides and polychlorobiphenyls) and telomere length in breeding adult black-legged kittiwakes (Rissa tridactyla), an arctic seabird species. Our results show that among legacy POPs, only blood concentration of oxychlordane, the major metabolite of chlordane mixture, is associated with shorter telomere length in females but not in males. This suggests that female kittiwakes could be more sensitive to oxychlordane, potentially explaining the previously reported lower survival rate in most oxychlordane-contaminated kittiwakes from the same population. This study is the first to report a significant and negative relationship between POPs and telomere length in a free-living bird and highlights sex-related susceptibility to banned pesticides.

Endocrine consequences of an acute stress under different thermal conditions: A study of corticosterone, prolactin, and thyroid hormones in the pigeon (Columbia livia).

In the context of global change, the physiological and hormonal stress responses have received much attention because of their implications in terms of allostasis. However, most studies have focused on glucocorticoids only as the "common" response to stressors while neglecting other endocrine axes and hormones (e.g. prolactin, thyroid hormones) that play a crucial role in metabolic adjustments. Interestingly, the responsiveness of all these endocrine axes to stress may depend on the energetic context and this context-dependent stress response has been overlooked so far. In the wild, temperature can vary to a large extent within a short time window and ambient temperature may affect these metabolic-related endocrine axes, and potentially, their responsiveness to an acute stressor. Here, we explicitly tested this hypothesis by examining the effect of a standardized stress protocol on multiple hormonal responses in the rock pigeon (Columbia livia). We tested the effect of an acute restraint stress on (1) corticosterone levels, (2) prolactin levels, and (3) thyroid hormone levels (triiodothyronine, thyroxine) in pigeons that were held either at cool temperature (experimental birds) or at room temperature (control birds) during the stress protocol. Although we found a significant influence of restraint stress on most hormone levels (corticosterone, prolactin, and thyroxine), triiodothyronine levels were not affected by the restraint stress. This demonstrates that stressors can have significant impact on multiple endocrine mechanisms. Importantly, all of these hormonal responses to stress were not affected by temperature, demonstrating that the exposure to cold temperature does not affect the way these hormone levels change in response to handling stress. This suggests that some endocrine responses to temperature decreases may be overridden by the endocrine responses to an acute restraint stress.