Concurrent threats and extinction risk in a long-lived, highly fecund vertebrate with parental care.

Detecting declines and quantifying extinction risk of long-lived, highly fecund vertebrates, including fishes, reptiles, and amphibians, can be challenging. In addition to the false notion that large clutches always buffer against population declines, the imperiled status of long-lived species can often be masked by extinction debt, wherein adults persist on the landscape for several years after populations cease to be viable. Here we develop a demographic model for the eastern hellbender (Cryptobranchus alleganiensis), an imperiled aquatic salamander with paternal care. We examined the individual and interactive effects of three of the leading threats hypothesized to contribute to the species' demise: habitat loss due to siltation, high rates of nest failure, and excess adult mortality caused by fishing and harvest. We parameterized the model using data on their life history and reproductive ecology to model the fates of individual nests and address multiple sources of density-dependent mortality under both deterministic and stochastic environmental conditions. Our model suggests that high rates of nest failure observed in the field are sufficient to drive hellbender populations toward a geriatric age distribution and eventually to localized extinction but that this process takes decades. Moreover, the combination of limited nest site availability due to siltation, nest failure, and stochastic adult mortality can interact to increase the likelihood and pace of extinction, which was particularly evident under stochastic scenarios. Density dependence in larval survival and recruitment can severely hamper a population's ability to recover from declines. Our model helps to identify tipping points beyond which extinction becomes certain and management interventions become necessary. Our approach can be generalized to understand the interactive effects of various threats to the extinction risk of other long-lived vertebrates. As we face unprecedented rates of environmental change, holistic approaches incorporating multiple concurrent threats and their impacts on different aspects of life history will be necessary to proactively conserve long-lived species.

Demographic feedbacks during evolutionary rescue can slow or speed adaptive evolution.

Populations declining toward extinction can persist via genetic adaptation in a process called evolutionary rescue. Predicting evolutionary rescue has applications ranging from conservation biology to medicine, but requires understanding and integrating the multiple effects of a stressful environmental change on population processes. Here we derive a simple expression for how generation time, a key determinant of the rate of evolution, varies with population size during evolutionary rescue. Change in generation time is quantitatively predicted by comparing how intraspecific competition and the source of maladaptation each affect the rates of births and deaths in the population. Depending on the difference between two parameters quantifying these effects, the model predicts that populations may experience substantial changes in their rate of adaptation in both positive and negative directions, or adapt consistently despite severe stress. These predictions were then tested by comparison to the results of individual-based simulations of evolutionary rescue, which validated that the tolerable rate of environmental change varied considerably as described by analytical results. We discuss how these results inform efforts to understand wildlife disease and adaptation to climate change, evolution in managed populations and treatment resistance in pathogens.

Size-dependence of food intake and mortality interact with temperature and seasonality to drive diversity in fish life histories.

Understanding how growth and reproduction will adapt to changing environmental conditions is a fundamental question in evolutionary ecology, but predicting the responses of specific taxa is challenging. Analyses of the physiological effects of climate change upon life history evolution rarely consider alternative hypothesized mechanisms, such as size-dependent foraging and the risk of predation, simultaneously shaping optimal growth patterns. To test for interactions between these mechanisms, we embedded a state-dependent energetic model in an ecosystem size-spectrum to ask whether prey availability (foraging) and risk of predation experienced by individual fish can explain observed diversity in life histories of fishes. We found that asymptotic growth emerged from size-based foraging and reproductive and mortality patterns in the context of ecosystem food web interactions. While more productive ecosystems led to larger body sizes, the effects of temperature on metabolic costs had only small effects on size. To validate our model, we ran it for abiotic scenarios corresponding to the ecological lifestyles of three tuna species, considering environments that included seasonal variation in temperature. We successfully predicted realistic patterns of growth, reproduction, and mortality of all three tuna species. We found that individuals grew larger when environmental conditions varied seasonally, and spawning was restricted to part of the year (corresponding to their migration from temperate to tropical waters). Growing larger was advantageous because foraging and spawning opportunities were seasonally constrained. This mechanism could explain the evolution of gigantism in temperate tunas. Our approach addresses variation in food availability and individual risk as well as metabolic processes and offers a promising approach to understand fish life-history responses to changing ocean conditions.

Filial Cannibalism Leads to Chronic Nest Failure of Eastern Hellbender Salamanders (Cryptobranchus alleganiensis).

AbstractIn species that provide parental care, parents will sometimes cannibalize their own young (i.e., filial cannibalism). Here, we quantified the frequency of whole-clutch filial cannibalism in a species of giant salamander (eastern hellbender; Cryptobranchus alleganiensis) that has experienced precipitous population declines with unknown causes. We used underwater artificial nesting shelters deployed across a gradient of upstream forest cover to assess the fates of 182 nests at 10 sites over 8 years. We found strong evidence that nest failure rates increased at sites with low riparian forest cover in the upstream catchment. At several sites, reproductive failure was 100%, mainly due to cannibalism by the caring male. The high incidence of filial cannibalism at degraded sites was not explained by evolutionary hypotheses for filial cannibalism based on poor adult body condition or low reproductive value of small clutches. Instead, larger clutches at degraded sites were most vulnerable to cannibalism. We hypothesize that high frequencies of filial cannibalism of large clutches in areas with low forest cover could be related to changes in water chemistry or siltation that influence parental physiology or that reduce the viability of eggs. Importantly, our results identify chronic nest failure as a possible mechanism contributing to population declines and observed geriatric age structure in this imperiled species.

Conservation successes and challenges for wide-ranging sharks and rays.

Overfishing is the most significant threat facing sharks and rays. Given the growth in consumption of seafood, combined with the compounding effects of habitat loss, climate change, and pollution, there is a need to identify recovery paths, particularly in poorly managed and poorly monitored fisheries. Here, we document conservation through fisheries management success for 11 coastal sharks in US waters by comparing population trends through a Bayesian state-space model before and after the implementation of the 1993 Fisheries Management Plan for Sharks. We took advantage of the spatial and temporal gradients in fishing exposure and fisheries management in the Western Atlantic to analyze the effect on the Red List status of all 26 wide-ranging coastal sharks and rays. We show that extinction risk was greater where fishing pressure was higher, but this was offset by the strength of management engagement (indicated by strength of National and Regional Plan of Action for sharks and rays). The regional Red List Index (which tracks changes in extinction risk through time) declined in all regions until the 1980s but then improved in the North and Central Atlantic such that the average extinction risk is currently half that in the Southwest. Many sharks and rays are wide ranging, and successful fisheries management in one country can be undone by poorly regulated or unregulated fishing elsewhere. Our study underscores that well-enforced, science-based management of carefully monitored fisheries can achieve conservation success, even for slow-growing species.

Sharkipedia: a curated open access database of shark and ray life history traits and abundance time-series.

A curated database of shark and ray biological data is increasingly necessary both to support fisheries management and conservation efforts, and to test the generality of hypotheses of vertebrate macroecology and macroevolution. Sharks and rays are one of the most charismatic, evolutionary distinct, and threatened lineages of vertebrates, comprising around 1,250 species. To accelerate shark and ray conservation and science, we developed Sharkipedia as a curated open-source database and research initiative to make all published biological traits and population trends accessible to everyone. Sharkipedia hosts information on 58 life history traits from 274 sources, for 170 species, from 39 families, and 12 orders related to length (n = 9 traits), age (8), growth (12), reproduction (19), demography (5), and allometric relationships (5), as well as 871 population time-series from 202 species. Sharkipedia relies on the backbone taxonomy of the IUCN Red List and the bibliography of Shark-References. Sharkipedia has profound potential to support the rapidly growing data demands of fisheries management, international trade regulation as well as anchoring vertebrate macroecology and macroevolution.

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour-polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph-specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome-wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi-niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans-species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations.

Does a complex life cycle affect adaptation to environmental change? Genome-informed insights for characterizing selection across complex life cycle.

Complex life cycles, in which discrete life stages of the same organism differ in form or function and often occupy different ecological niches, are common in nature. Because stages share the same genome, selective effects on one stage may have cascading consequences through the entire life cycle. Theoretical and empirical studies have not yet generated clear predictions about how life cycle complexity will influence patterns of adaptation in response to rapidly changing environments or tested theoretical predictions for fitness trade-offs (or lack thereof) across life stages. We discuss complex life cycle evolution and outline three hypotheses-ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy-for how selection may operate on organisms with complex life cycles. We suggest a within-generation experimental design that promises significant insight into composite selection across life cycle stages. As part of this design, we conducted simulations to determine the power needed to detect selection across a life cycle using a population genetic framework. This analysis demonstrated that recently published studies reporting within-generation selection were underpowered to detect small allele frequency changes (approx. 0.1). The power analysis indicates challenging but attainable sampling requirements for many systems, though plants and marine invertebrates with high fecundity are excellent systems for exploring how organisms with complex life cycles may adapt to climate change.

Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only "sneak" spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production.

Half a century of global decline in oceanic sharks and rays.

Overfishing is the primary cause of marine defaunation, yet declines in and increasing extinction risks of individual species are difficult to measure, particularly for the largest predators found in the high seas1-3. Here we calculate two well-established indicators to track progress towards Aichi Biodiversity Targets and Sustainable Development Goals4,5: the Living Planet Index (a measure of changes in abundance aggregated from 57 abundance time-series datasets for 18 oceanic shark and ray species) and the Red List Index (a measure of change in extinction risk calculated for all 31 oceanic species of sharks and rays). We find that, since 1970, the global abundance of oceanic sharks and rays has declined by 71% owing to an 18-fold increase in relative fishing pressure. This depletion has increased the global extinction risk to the point at which three-quarters of the species comprising this functionally important assemblage are threatened with extinction. Strict prohibitions and precautionary science-based catch limits are urgently needed to avert population collapse6,7, avoid the disruption of ecological functions and promote species recovery8,9.

Relationships between Pacific salmon and aquatic and terrestrial ecosystems: implications for ecosystem-based management.

Pacific salmon influence temperate terrestrial and freshwater ecosystems through the dispersal of marine-derived nutrients and ecosystem engineering of stream beds when spawning. They also support large fisheries, particularly along the west coast of North America. We provide a comprehensive synthesis of relationships between the densities of Pacific salmon and terrestrial and aquatic ecosystems, summarize the direction, shape, and magnitude of these relationships, and identify possible ecosystem-based management indicators and benchmarks. We found 31 studies that provided 172 relationships between salmon density (or salmon abundance) and species abundance, species diversity, food provisioning, individual growth, concentration of marine-derived isotopes, nutrient enhancement, phenology, and several other ecological responses. The most common published relationship was between salmon density and marine-derived isotopes (40%), whereas very few relationships quantified ecosystem-level responses (5%). Only 13% of all relationships tended to reach an asymptote (i.e., a saturating response) as salmon densities increased. The number of salmon killed by bears and the change in biomass of different stream invertebrate taxa between spawning and nonspawning seasons were relationships that usually reached saturation. Approximately 46% of all relationships were best described with linear or curved nonasymptotic models, indicating a lack of saturation. In contrast, 41% of data sets showed no relationship with salmon density or abundance, including many of the relationships with stream invertebrate and biofilm biomass density, marine-derived isotope concentrations, or vegetation density. Bears required the highest densities of salmon to reach their maximum observed food consumption (i.e., 9.2 kg/m2 to reach the 90% threshold of the relationship's asymptote), followed by freshwater fish abundance (90% threshold = 7.3 kg/m2 of salmon). Although the effects of salmon density on ecosystems are highly varied, it appears that several of these relationships, such as bear food consumption, could be used to develop indicators and benchmarks for ecosystem-based fisheries management.

Global reconstruction of life-history strategies: A case study using tunas.

Measuring the demographic parameters of exploited populations is central to predicting their vulnerability and extinction risk. However, current rates of population decline and species loss greatly outpace our ability to empirically monitor all populations that are potentially threatened.The scale of this problem cannot be addressed through additional data collection alone, and therefore it is a common practice to conduct population assessments based on surrogate data collected from similar species. However, this approach introduces biases and imprecisions that are difficult to quantify. Recent developments in hierarchical modelling have enabled missing values to be reconstructed based on the correlations between available life-history data, linking similar species based on phylogeny and environmental conditions.However, these methods cannot resolve life-history variability among populations or species that are closely placed spatially or taxonomically. Here, theoretically motivated constraints that align with life-history theory offer a new avenue for addressing this problem. We describe a Bayesian hierarchical approach that combines fragmented, multispecies and multi-population data with established life-history theory, in order to objectively determine similarity between populations based on trait correlations (life-history trade-offs) obtained from model fitting.We reconstruct 59 unobserved life-history parameters for 23 populations of tuna that sustain some of the world's most valuable fisheries. Testing by cross-validation across different scenarios indicated that life-histories were accurately reconstructed when information was available for other populations of the same species. The reconstruction of several traits was also accurate for species represented by a single population, although credible intervals increased dramatically. Synthesis and applications. The described Bayesian hierarchical method provides access to life-history traits that are difficult to measure directly and reconstructs missing life-history information useful for assessing populations and species that are directly or indirectly affected by human exploitation of natural resources. The method is particularly useful for examining populations that are spatially or taxonomically similar, and the reconstructed life-history strategies described for the principal market tunas have immediate application to the world-wide management of these fisheries.

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males.

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full-sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male-controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.

Overcoming the Data Crisis in Biodiversity Conservation.

How can we track population trends when monitoring data are sparse? Population declines can go undetected, despite ongoing threats. For example, only one of every 200 harvested species are monitored. This gap leads to uncertainty about the seriousness of declines and hampers effective conservation. Collecting more data is important, but we can also make better use of existing information. Prior knowledge of physiology, life history, and community ecology can be used to inform population models. Additionally, in multispecies models, information can be shared among taxa based on phylogenetic, spatial, or temporal proximity. By exploiting generalities across species that share evolutionary or ecological characteristics within Bayesian hierarchical models, we can fill crucial gaps in the assessment of species' status with unparalleled quantitative rigor.

Growth, productivity, and relative extinction risk of a data-sparse devil ray.

Devil rays (Mobula spp.) face intensifying fishing pressure to meet the ongoing international demand for gill plates. The paucity of information on growth, mortality, and fishing effort for devil rays make quantifying population growth rates and extinction risk challenging. Furthermore, unlike manta rays (Manta spp.), devil rays have not been listed on CITES. Here, we use a published size-at-age dataset for the Spinetail Devil Ray (Mobula japanica), to estimate somatic growth rates, age at maturity, maximum age, and natural and fishing mortality. We then estimate a plausible distribution of the maximum intrinsic population growth rate (rmax) and compare it to 95 other chondrichthyans. We find evidence that larger devil ray species have low somatic growth rate, low annual reproductive output, and low maximum population growth rates, suggesting they have low productivity. Fishing rates of a small-scale artisanal Mexican fishery were comparable to our estimate of rmax, and therefore probably unsustainable. Devil ray rmax is very similar to that of manta rays, indicating devil rays can potentially be driven to local extinction at low levels of fishing mortality and that a similar degree of protection for both groups is warranted.

Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon.

Large male body size is typically favored by directional sexual selection through competition for mates. However, alternative male life-history phenotypes, such as "sneakers," should decrease the strength of sexual selection acting on body size of large "fighter" males. We tested this prediction with salmon species; in southern populations, where sneakers are common, fighter males should be smaller than in northern populations, where sneakers are rare, leading to geographical clines in sexual size dimorphism (SSD). Consistent with our prediction, fighter male body size and SSD (fighter male∶female size) increase with latitude in species with sneaker males (Atlantic salmon Salmo salar and masu salmon Oncorhynchus masou) but not in species without sneakers (chum salmon Oncorhynchus keta and pink salmon Oncorhynchus gorbuscha). This is the first evidence that sneaker males affect SSD across populations and species, and it suggests that alternative male mating strategies may shape the evolution of body size.

Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon.

Species' life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage-structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co-variation in salmonids, we generate new hypotheses for the evolution of trade-offs among life history traits.

Ten principles from evolutionary ecology essential for effective marine conservation.

Sustainably managing marine species is crucial for the future health of the human population. Yet there are diverse perspectives concerning which species can be exploited sustainably, and how best to do so. Motivated by recent debates in the published literature over marine conservation challenges, we review ten principles connecting life-history traits, population growth rate, and density-dependent population regulation. We introduce a framework for categorizing life histories, POSE (Precocial-Opportunistic-Survivor-Episodic), which illustrates how a species' life-history traits determine a population's compensatory capacity. We show why considering the evolutionary context that has shaped life histories is crucial to sustainable management. We then review recent work that connects our framework to specific opportunities where the life-history traits of marine species can be used to improve current conservation practices.

Multiple mating and reproductive skew in parental and introgressed females of the live-bearing fish Xiphophorus birchmanni.

Just as mating patterns can promote speciation or hybridization, the presence of hybridization can shape mating patterns within a population. In this study, we characterized patterns of multiple mating and reproductive skew in a naturally hybridizing swordtail fish species, Xiphophorus birchmanni. We quantified multiple mating using microsatellite markers to genotype embryos from 43 females collected from 2 wild populations. We also used a suite of single-nucleotide polymorphism markers to categorize females and their inferred mates as either parental X. birchmanni or as introgressed individuals, which carried alleles from a sister species, X. malinche. We found that parental and introgressed X. birchmanni females mated multiply with both parental and introgressed males. We found no difference in mating patterns or reproductive skew between parental and introgressed X. birchmanni females. However, nonintrogressed X. birchmanni males mated more often with large, fecund females. These females also had the greatest levels of skew in fertilization success of males. Thus, our results show that X. birchmanni has a polygynandrous mating system and that introgression of X. malinche alleles has only subtle effects on mating patterns in this species.