Environmental Cues and Mechanisms Underpinning Sex Change in Fish.

Fishes are the only vertebrates that undergo sex change during their lifetime, but even within this group, a unique reproductive strategy is displayed by only 1.5% of the teleosts. This lability in alternating sexual fate is the result of the simultaneous suppression and activation of opposing male and female networks. Here, we provide a brief review summarizing recent advances in our understanding of the environmental cues that trigger sex change and their perception, integration, and translation into molecular cascades that convert the sex of an individual. We particularly focus on molecular events underpinning the complex behavioral and morphological transformation involved in sex change, dissecting the main molecular players and regulatory networks that shape the transformation of one sex into the opposite. We show that histological changes and molecular pathways governing gonadal reorganization are better described than the neuroendocrine basis of sex change and that, despite important advances, information is lacking for the majority of hermaphrodite species. We highlight significant gaps in our knowledge of how sex change takes place and suggest future research directions.

Genomic landscape of geographically structured colour polymorphism in a temperate marine fish.

The study of phenotypic variation patterns among populations is fundamental to elucidate the drivers of evolutionary processes. Empirical evidence that supports ongoing genetic divergence associated with phenotypic variation remains very limited for marine species where larval dispersal is a common homogenizing force. We present a genome-wide analysis of a marine fish, Labrus bergylta, comprising 144 samples distributed from Norway to Spain, a large geographical area that harbours a gradient of phenotypic differentiation. We analysed 39,602 biallelic single nucleotide polymorphisms and found a clear latitudinal gradient of genomic differentiation strongly correlated with the variation in phenotypic morph frequencies observed across the North Atlantic. We also detected a strong association between the latitude and the number of loci that appear to be under divergent selection, which increased with differences in coloration but not with overall genetic differentiation. Our results demonstrate that strong reproductive isolation is occurring between sympatric colour morphs of L. bergylta found at the southern areas and provide important new insights into the genomic changes shaping early stages of differentiation that might precede speciation with gene flow.

New insights in oocyte dynamics shed light on the complexities associated with fish reproductive strategies.

Information on temporal variations in stock reproductive potential (SRP) is essential in fisheries management. Despite this relevance, fundamental understanding of egg production variability remains largely unclear due to difficulties in tracking the underlying complex fluctuations in early oocyte recruitment that determines fecundity. We applied advanced oocyte packing density theory to get in-depth, quantitative insights across oocyte stages and seasons, selecting the commercially valuable European hake (Merluccius merluccius) as a case study. Our work evidenced sophisticated seasonal oocyte recruitment dynamics and patterns, mostly driven by a low-cost predefinition of fecundity as a function of fish body size, likely influenced also by environmental cues. Fecundity seems to be defined at a much earlier stage of oocyte development than previously thought, implying a quasi-determinate - rather than indeterminate - fecundity type in hake. These results imply a major change in the conceptual approach to reproductive strategies in teleosts. These findings not only question the current binary classification of fecundity as either determinate or indeterminate, but also suggest that current practices regarding potential fecundity estimation in fishes should be complemented with studies on primary oocyte dynamics. Accordingly, the methodology and approach adopted in this study may be profitably applied for unravelling some of the complexities associated with oocyte recruitment and thereby SRP variability.

Historical gene flow constraints in a northeastern Atlantic fish: phylogeography of the ballan wrasse Labrus bergylta across its distribution range.

The distribution and demographic patterns of marine organisms in the north Atlantic were largely shaped by climatic changes during the Pleistocene, when recurrent glacial maxima forced them to move south or to survive in northern peri-glacial refugia. These patterns were also influenced by biological and ecological factors intrinsic to each species, namely their dispersion ability. The ballan wrasse (Labrus bergylta), the largest labrid fish along Europe's continental margins, is a target for fisheries and aquaculture industry. The phylogeographic pattern, population structure, potential glacial refugia and recolonization routes for this species were assessed across its full distribution range, using mitochondrial and nuclear markers. The existence of a marked population structure can reflect both recolonization from three distinct glacial refugia and current and past oceanographic circulation patterns. Although isolated in present times, shared haplotypes between continental and Azores populations and historical exchange of migrants in both directions point to a common origin of L. bergylta. This situation is likely to be maintained and/or accentuated by current circulation patterns in the north Atlantic, and may lead to incipient speciation in the already distinct Azorean population. Future monitoring of this species is crucial to evaluate how this species is coping with current environmental changes.

Sex Change in Clownfish: Molecular Insights from Transcriptome Analysis.

Sequential hermaphroditism is a unique reproductive strategy among teleosts that is displayed mainly in fish species living in the coral reef environment. The reproductive biology of hermaphrodites has long been intriguing; however, very little is known about the molecular pathways underlying their sex change. Here, we provide the first de novo transcriptome analyses of a hermaphrodite teleost´s undergoing sex change in its natural environment. Our study has examined relative gene expression across multiple groups-rather than just two contrasting conditions- and has allowed us to explore the differential expression patterns throughout the whole process. Our analysis has highlighted the rapid and complex genomic response of the brain associated with sex change, which is subsequently transmitted to the gonads, identifying a large number of candidate genes, some well-known and some novel, involved in the process. The present study provides strong evidence of the importance of the sex steroidogenic machinery during sex change in clownfish, with the aromatase gene playing a central role, both in the brain and the gonad. This work constitutes the first genome-wide study in a social sex-changing species and provides insights into the genetic mechanism governing social sex change and gonadal restructuring in protandrous hermaphrodites.

Contrasting evolutionary demography induced by fishing: the role of adaptive phenotypic plasticity.

Mounting evidence now shows that fishing activity modifies both heritable life-history traits and ecological processes in harvested populations. However, ecological and evolutionary changes are intimately linked and can occur on the same time scale, and few studies have investigated their combined effect on fish population dynamics. Here, we contrast two population subunits of a harvested fish species in the Northeast Atlantic, the European hake (Merluccius merluccius), in the light of the emerging field of evolutionary demography, which considers the interacting processes between ecology and evolution. The two subunits experienced similar age/size truncation due to size-selective fishing, but displayed differences in key ecological processes (recruitment success) and phenotypic characteristics (maturation schedule). We investigate how temporal variation in maturation and recruitment success interactively shape the population dynamics of the two subunits. We document that the two subunits of European hake displayed different responses to fishing in maturation schedules, possibly because of the different level of adaptive phenotypic plasticity. Our results also suggest that high phenotypic plasticity can dampen the effects of fisheries-induced demographic truncation on population dynamics, whereas a population subunit characterized by low phenotypic plasticity may suffer from additive effects of ecological and life-history responses. Similar fishing pressure may thus trigger contrasting interactions between life history variation and ecological processes within the same population. The presented findings improve our understanding of how fishing impacts eco-evolutionary dynamics, which is a keystone for a more comprehensive management of harvested species.

Demographic variation between colour patterns in a temperate protogynous hermaphrodite, the ballan wrasse Labrus bergylta.

Fish populations are often treated as homogeneous units in typical fishery management, thereby tacitly ignoring potential intraspecific variation which can lead to imprecise management rules. However, intraspecific variation in life-history traits is widespread and related to a variety of factors. We investigated the comparative age-based demography of the two main colour patterns of Labrus bergylta (plain and spotted, which coexist in sympatry), a commercially valuable resource in the NE Atlantic. Individuals were aged based on otolith readings after validating the annual periodicity of annuli deposition. The relationships between the otolith weight and fish age and between otolith length and fish length were strong but differed between colour patterns. The fit of the growth models to the age and length data resulted in divergent growth curves between colour morphotypes and between sexes. Males and spotted individuals attained larger mean asymptotic sizes (Linf ) than females and plain individuals, respectively, but converged to them more slowly (smaller k). Estimates of mortality based on catch curves from two independent datasets provided a global total mortality (Z) of 0.35 yr(-1), although Z was larger in plain and female individuals. Overall, the results of this research have direct implications for management of L. bergylta and, as a precautionary measure, we recommend considering both colour patterns as two different management units.

Comparison of demographic and direct methods to calculate probabilistic maturation reaction norms for Flemish Cap cod (Gadus morhua).

Age and length at maturation have declined in many fish populations and this has been hypothesized to be a genetic change caused by high fishing mortality. Probabilistic Maturation Reaction Norms (PMRNs) have been used as a tool to gain a better understanding of the possible genetic nature of these changes. The demographic and direct methods are two ways to calculate PMRNs. The data requirements are more often met for the demographic method than for the direct method which requires the identification of recruit spawners. However, the demographic method relies on more assumptions than the direct method, typically assuming equality of growth and mortality rates for immature and mature individuals within an age class. This study provides the first direct comparison of demographic and direct methods and shows that both methods produce comparable results. Differences between methods are hypothesized to be owed to possible differences in growth rate between mature and immature individuals in Flemish Cap cod.

Endocrine alteration and other biochemical responses in juvenile turbot exposed to the Prestige fuel oil.

Juvenile turbot (Scophthalmus maximus) were exposed to different concentrations of the Prestige fuel oil through the diet. The effects on hepatic biotransformation enzymes, namely, 7-ethoxyresorufin O-deethylase (EROD), catalase, and phase II activities - UDP-glucuronosyltransferases (UGT) and cytosolic sulfotransferases (SULT) -, were monitored after 42-day exposure. Additionally, potential alterations on the endocrine system of juvenile turbot were assessed by measuring circulating levels of testosterone and 17beta-estradiol in plasma, together with gonadal P450 aromatase activity and the glucuronidation of testosterone by liver microsomal fractions. Fluorescent aromatic compounds (FACs) in bile were determined as an indicator of exposure to polycyclic aromatic hydrocarbons (PAHs). EROD activity increased in a dose dependent manner, and a positive correlation between levels of FACs in bile and EROD activity was observed. A significant increase in UGT activity was observed in fish exposed to medium and high fuel doses, whereas SULT cytosolic activity was not responsive to exposure. Exposure to the Prestige fuel oil sharply reduced circulating levels of testosterone in plasma. The obtained results suggest the ability of the Prestige fuel oil to alter hepatic biotransformation enzymes and to disrupt endogenous hormone levels in juvenile turbot, with unknown consequences in terms of sexual differentiation and reproduction.

Use of multivariate analysis to assess the nutritional condition of fish larvae from nucleic acids and protein content.

The nutritional condition of turbot larvae (Scophthalmus maximus) was assessed by a multivariate analysis with DNA, RNA, and protein content as input variables. Special attention was given to the time that feeding began and to the timing and duration of starvation. The combination of the principal components analysis and the stepwise discriminant analysis, both techniques of multivariate analysis, made it possible to allocate the larvae into groups that were defined and identified based on similarities in developmental stage and nutritional condition. The developmental stage was mostly determined by the input variables DNA and protein content, while nutritional condition was determined by the RNA content. In the period studied, the more developed larvae were less resistant to starvation. Furthermore, when initial feeding was delayed as little as 6 h, the variables analyzed were markedly changed, and the effect on the deprived larvae was found to be equivalent to a 3-day delay in development-when compared with the larvae fed immediately after mouth opening. Through this technique, new samples of larvae with unknown history might be classified into groups, using their DNA, RNA, and protein content as input values in the defined classification functions. Results were compared to those obtained using RNA/DNA and RNA/dry weight indices, and the multivariate method was considered to be more sensitive and to provide extra information about larval nutritional history and development.