Sébastien Nusslé

Evolutionary impact assessment: accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management

Managing fisheries resources to maintain healthy ecosystems is one of the main goals of the ecosystem approach to fisheries (EAF). While a number of international treaties call for the implementation of EAF, there are still gaps in the underlying methodology. One aspect that has received substantial scientific attention recently is fisheries-induced evolution (FIE). Increasing evidence indicates that intensive fishing has the potential to exert strong directional selection on life-history traits, behaviour, physiology, and morphology of exploited fish. Of particular concern is that reversing evolutionary responses to fishing can be much more difficult than reversing demographic or phenotypically plastic responses. Furthermore, like climate change, multiple agents cause FIE, with effects accumulating over time. Consequently, FIE may alter the utility derived from fish stocks, which in turn can modify the monetary value living aquatic resources provide to society. Quantifying and predicting the evolutionary effects of fishing is therefore important for both ecological and economic reasons. An important reason this is not happening is the lack of an appropriate assessment framework. We therefore describe the evolutionary impact assessment (EvoIA) as a structured approach for assessing the evolutionary consequences of fishing and evaluating the predicted evolutionary outcomes of alternative management options. EvoIA can contribute to EAF by clarifying how evolution may alter stock properties and ecological relations, support the precautionary approach to fisheries management by addressing a previously overlooked source of uncertainty and risk, and thus contribute to sustainable fisheries.

Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events

Significance Mass mortality events (MMEs), the rapid, catastrophic die-off of organisms, are an example of a rare event affecting natural populations. Individual reports of MMEs clearly demonstrate their ecological and evolutionary importance, yet our understanding of the general features characterizing such events is limited. Here, we conducted the first, to our knowledge, quantitative analysis of MMEs across the animal kingdom, and as such, we were able to explore novel patterns, trends, and features associated with MMEs. Our analysis uncovered the surprising finding that there have been recent shifts in the magnitudes of MMEs and their associated causes. Our database allows the recommendation of improvements for data collection in ways that will enhance our understanding of how MMEs relate to ongoing perturbations to ecosystems. Mass mortality events (MMEs) are rapidly occurring catastrophic demographic events that punctuate background mortality levels. Individual MMEs are staggering in their observed magnitude: removing more than 90% of a population, resulting in the death of more than a billion individuals, or producing 700 million tons of dead biomass in a single event. Despite extensive documentation of individual MMEs, we have no understanding of the major features characterizing the occurrence and magnitude of MMEs, their causes, or trends through time. Thus, no framework exists for contextualizing MMEs in the wake of ongoing global and regional perturbations to natural systems. Here we present an analysis of 727 published MMEs from across the globe, affecting 2,407 animal populations. We show that the magnitude of MMEs has been intensifying for birds, fishes, and marine invertebrates; invariant for mammals; and decreasing for reptiles and amphibians. These shifts in magnitude proved robust when we accounted for an increase in the occurrence of MMEs since 1940. However, it remains unclear whether the increase in the occurrence of MMEs represents a true pattern or simply a perceived increase. Regardless, the increase in MMEs appears to be associated with a rise in disease emergence, biotoxicity, and events produced by multiple interacting stressors, yet temporal trends in MME causes varied among taxa and may be associated with increased detectability. In addition, MMEs with the largest magnitudes were those that resulted from multiple stressors, starvation, and disease. These results advance our understanding of rare demographic processes and their relationship to global and regional perturbations to natural systems.

Causal mechanisms underlying host specificity in bat ectoparasites

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.

Fishery-induced selection on an Alpine whitefish: quantifying genetic and environmental effects on individual growth rate

Size‐selective fishing, environmental changes and reproductive strategies are expected to affect life‐history traits such as the individual growth rate. The relative contribution of these factors is not clear, particularly whether size‐selective fishing can have a substantial impact on the genetics and hence on the evolution of individual growth rates in wild populations. We analysed a 25‐year monitoring survey of an isolated population of the Alpine whitefish Coregonus palaea. We determined the selection differentials on growth rate, the actual change of growth rate over time and indicators of reproductive strategies that may potentially change over time. The selection differential can be reliably estimated in our study population because almost all the fish are harvested within their first years of life, i.e. few fish escape fishing mortality. We found a marked decline in average adult growth rate over the 25 years and a significant selection differential for adult growth, but no evidence for any linear change in reproductive strategies over time. Assuming that the heritability of growth in this whitefish corresponds to what was found in other salmonids, about a third of the observed decline in growth rate would be linked to fishery‐induced evolution. Size‐selective fishing seems to affect substantially the genetics of individual growth in our study population.

Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity–energy budgets

Anthropogenic disturbance of wildlife is of growing conservation concern, but we lack comprehensive approaches of its multiple negative effects. We investigated several effects of disturbance by winter outdoor sports on free-ranging alpine Black Grouse by simultaneously measuring their physiological and behavioral responses. We experimentally flushed radio-tagged Black Grouse from their snow burrows, once a day, during several successive days, and quantified their stress hormone levels (corticosterone metabolites in feces [FCM] collected. from individual snow burrows). We also measured feeding time allocation (activity budgets reconstructed from radio-emitted signals) in response to anthropogenic disturbance. Finally, we estimated the related extra energy expenditure that may be incurred: based on activity budgets, energy expenditure was modeled from measures of metabolism obtained from captive birds subjected to different ambient temperatures. The pattern of FCM excretion indicated the existence of a funneling effect as predicted by the allostatic theory of stress: initial stress hormone concentrations showed a wide inter-individual variation, which decreased during experimental flushing. Individuals with low initial pre-flushing FCM values augmented their concentration, while individuals with high initial FCM values lowered it. Experimental disturbance resulted in an extension of feeding duration during the following evening foraging bout, confirming the prediction that Black Grouse must compensate for the extra energy expenditure elicited by human disturbance. Birds with low initial baseline FCM concentrations were those that spent more time foraging. These FCM excretion and foraging patterns suggest that birds with high initial FCM concentrations might have been experiencing a situation of allostatic overload. The energetic model provides quantitative estimates of extra energy expenditure. A longer exposure to ambient temperatures outside the shelter of snow burrows, following disturbance, could increase the daily energy expenditure by > 10%, depending principally on ambient temperature and duration of exposure. This study confirms the predictions of allostatic theory and, to the best of our knowledge, constitutes the first demonstration of a funneling effect. It further establishes that winter recreation activities incur costly allostatic behavioral and energetic adjustments, which call for the creation of winter refuge areas together with the implementation of visitor-steering measures for sensitive wildlife.

New vineyard cultivation practices create patchy ground vegetation, favouring Woodlarks

AbstractIntensive agriculture, in which detrimental farming practices lessen food abundance and/or reduce food accessibility for many animal species, has led to a widespread collapse of farmland biodiversity. Vineyards in central and southern Europe are intensively cultivated; though they may still harbour several rare plant and animal species, they remain little studied. Over the past decades, there has been a considerable reduction in the application of insecticides in wine production, with a progressive shift to biological control (integrated production) and, to a lesser extent, organic production. Spraying of herbicides has also diminished, which has led to more vegetation cover on the ground, although most vineyards remain bare, especially in southern Europe. The effects of these potentially positive environmental trends upon biodiversity remain mostly unknown as regards vertebrates. The Woodlark (Lullula arborea) is an endangered, short-distance migratory bird that forages and breeds on the ground. In southern Switzerland (Valais), it occurs mostly in vineyards. We used radiotracking and mixed effects logistic regression models to assess Woodlark response to modern vineyard farming practices, study factors driving foraging micro-habitat selection, and determine optimal habitat profile to inform management. The presence of ground vegetation cover was the main factor dictating the selection of foraging locations, with an optimum around 55% at the foraging patch scale. These conditions are met in integrated production vineyards, but only when grass is tolerated on part of the ground surface, which is the case on ca. 5% of the total Valais vineyard area. In contrast, conventionally managed vineyards covering ≥95% of the vineyard area are too bare because of systematic application of herbicides all over the ground, whilst the rare organic vineyards usually have a too-dense sward. The optimal mosaic with ca. 50% ground vegetation cover is currently achieved in integrated production vineyards where herbicide is applied every second row. In organic production, ca. 50% ground vegetation cover should be promoted, which requires regular mechanical removal of ground vegetation. These measures are likely to benefit general biodiversity in vineyards.ZusammenfassungNeue Methoden im Weinbau schaffen lückige Bodenvegetation und fördern die Heidelerche Die Intensivlandwirtschaft, deren Anbaumethoden sich vielfach negativ auf die Nahrungsverfügbarkeit für viele Tierarten auswirken, hat zu einem großflächigen Rückgang der Biodiversität in Agrarlebensräumen geführt. In den Weinbaugebieten Zentral— und Südeuropas, die trotz intensiver Bewirtschaftung immer noch viele seltene Tier— und Pflanzenarten beherbergen, sind diese Zusammenhänge bisher nur wenig untersucht. In der Schweiz wurde die Anwendung von Insektiziden während der letzten Jahrzehnte stark reduziert, einhergehend mit einem Trend hin zur Integrierten Produktion (IP; biologische Schädlingskontrolle) und—in geringerem Umfang—biologischer Produktion (Bioweinbau). Auch die Verwendung von Herbiziden wurde eingeschränkt, was zu einer Zunahme der Bodenvegetation führte. Die Auswirkungen dieser potentiell biodiversitätsfördernden Trends auf die Wirbeltierfauna sind jedoch bisher unklar. Die Heidelerche (Lullula arborea), ein gefährdeter Kurz-strecken-zieher, der am Boden sowohl brütet als auch Nahrung sucht, kommt in der Südschweiz (Wallis) vorwiegend in Rebgebieten vor. Mit Hilfe von Radiotelemetrie und gemischten logistischen Regressionsmodellen untersuchten wir die Auswirkungen moderner Wein-anbau-methoden auf die Nahrungshabitatselektion der Heidelerche und bestimmten das optimale Habitatprofil als Grundlage für Managementempfehlungen. Bei der Nahrungssuche wurde die Habitatwahl hauptsächlich durch den Deckungsgrad der Bodenvegetation bestimmt, wobei das Optimum bei 55% lag. In Rebparzellen, die nach den Vorgaben der IP bewirtschaftet werden, sind diese Bedingungen erfüllt, wenn auf einem Teil der Fläche Grasbewuchs toleriert wird—dies ist jedoch auf weniger als 5% der gesamten Wein-Anbaufläche im Wallis der Fall. Herkömmlich bewirtschaftete Rebparzellen haben aufgrund der systematischen Anwendung von Herbiziden zuwenig Bodenvegetation, während die wenigen biologisch bewirtschafteten Rebparzellen eine zu dichte Bodenvegetation aufweisen. IP Rebparzellen, bei der eine Anwendung von Herbiziden in jeder zweiten Reihe von Weinstöcken ein alternierendes Muster von bewachsenen und unbewachsenen Reihen hervorbringt, scheinen sich damit vorteilhaft auf die Heidelerche auszuwirken. In biologisch bewirtschafteten Rebparzellen könnte dieser Mosaikeffekt durch eine teilweise, mechanische Entfernung der Bodenvegetation erreicht werden. Diese Maßnahme würde sehr wahrscheinlich auch allgemein zur Biodiversitätsförderung in Weinanbaugebieten beitragen.

Relationships of basal metabolic rate, relative testis size and cycle length of spermatogenesis in shrews (Mammalia, Soricidae)

The aim of the present study was to determinate the cycle length of spermatogenesis in three species of shrew, Suncus murinus, Sorex coronatus and Sorex minutus, and to assess the relative influence of variation in basal metabolic rate (BMR) and mating system (level of sperm competition) on the observed rate of spermatogenesis, including data of shrew species studied before (Sorex araneus, Crocidura russula and Neomys fodiens). The dynamics of sperm production were determined by tracing 5-bromodeoxyuridine in the DNA of germ cells. As a continuous scaling of mating systems is not evident, the level of sperm competition was evaluated by the significantly correlated relative testis size (RTS). The cycle durations estimated by linear regression were 14.3 days (RTS 0.3%) in Suncus murinus, 9.0 days (RTS 0.5%) in Sorex coronatus and 8.5 days (RTS 2.8%) in Sorex minutus. In regression and multiple regression analyses including all six studied species of shrew, cycle length was significantly correlated with BMR (r2=0.73) and RTS (r2=0.77). Sperm competition as an ultimate factor obviously leads to a reduction in the time of spermatogenesis in order to increase sperm production. BMR may act in the same way, independently or as a proximate factor, revealed by the covariation, but other factors (related to testes size and thus to mating system) may also be involved.

Testis size, sperm characteristics and testosterone concentrations in four species of shrews (Mammalia, Soricidae).

The aim of this study was to establish and compare the sperm characteristics in four shrew species in the context of the sperm competition hypothesis. As expected, the large relative testis size in promiscuous species was associated with a high number of cauda epididymal spermatozoa and a high concentration of circulating testosterone. In addition, in Sorex and Neomys, species with high intensity of sperm competition, the spermatozoa stored in cauda epididymis were characterized by high percentage of progressive motility whereas in Crocidura and Suncus, the cauda epididymal spermatozoa were motile but with very low percentage of progressive motility. This capability is achieved only following the passage through the vas gland, a specialized region for sperm storage located along the vas deferens in these shrew species. The hypothesis that sperm competition is positively correlated with spermatozoa length could not be confirmed. In Crocidura and Suncus, the total sperm length is increased by the large sperm head due to a big acrosome. This trait, specific to the subfamily Crocidurinae, may results from a selective pressure independent of the context of sperm competition, related to a specific, but as yet unclear role, for the acrosome during the fertilization.

Periconceptional folate consumption is associated with neonatal DNA methylation modifications in neural crest regulatory and cancer development genes

Folate deficiency during early embryonic development constitutes a risk factor for neural tube defects and potentially for childhood leukemia via unknown mechanisms. We tested whether folate consumption during the 12 months prior to conception induced DNA methylation modifications at birth in healthy neonates with a genome-wide and agnostic approach. We hypothesized that DNA methylation in genes involved in neural tube development and/or cancer susceptibility would be affected by folate exposure. We retrospectively assessed folate exposure at the time of conception by food-frequency questionnaires administered to the mothers of 343 healthy newborns. We measured genome-wide DNA methylation from neonatal blood spots. We implemented a method based on bootstrap resampling to decrease false-positive findings. Folate was inversely associated with DNA methylation throughout the genome. Among the top folate-associated genes that were replicated in an independent Gambian study were TFAP2A, a gene critical for neural crest development, STX11, a gene implicated in acute myeloid leukemia, and CYS1, a candidate gene for cystic kidney disease. Reduced periconceptional folate intake was associated with increased methylation and, in turn, decreased gene expression at these 3 loci. The top folate-sensitive genes defined by their associated CpG sites were enriched for numerous transcription factors by Gene Set Enrichment Analysis, including those implicated in cancer development (e.g., MYC-associated zinc finger protein). The influence of estimated periconceptional folate intake on neonatal DNA methylation levels provides potential mechanistic insights into the role of this vitamin in the development of neural tube defects and childhood cancers.

Cycle Length of Spermatogenesis in Shrews (Mammalia: Soricidae) with High and Low Metabolic Rates and Different Mating Systems

Abstract The aim of the present study was to establish and compare the durations of the seminiferous epithelium cycles of the common shrew Sorex araneus, which is characterized by a high metabolic rate and multiple paternity, and the greater white-toothed shrew Crocidura russula, which is characterized by a low metabolic rate and a monogamous mating system. Twelve S. araneus males and fifteen C. russula males were injected intraperitoneally with 5-bromodeoxyuridine, and the testes were collected. For cycle length determinations, we applied the classical method of estimation and linear regression as a new method. With regard to variance, and even with a relatively small sample size, the new method seems to be more precise. In addition, the regression method allows the inference of information for every animal tested, enabling comparisons of different factors with cycle lengths. Our results show that not only increased testis size leads to increased sperm production, but it also reduces the duration of spermatogenesis. The calculated cycle lengths were 8.35 days for S. araneus and 12.12 days for C. russula. The data obtained in the present study provide the basis for future investigations into the effects of metabolic rate and mating systems on the speed of spermatogenesis.