Maternal investment evolves with larger body size and higher diversification rate in sharks and rays.

Across vertebrates, live bearing evolved at least 150 times from ancestral egg laying into diverse forms and degrees of prepartum maternal investment.1,2 A key question is how reproductive diversity arose and whether reproductive diversification underlies species diversification.3,4,5,6,7,8,9,10,11 To test this, we evaluate the most basal jawed vertebrates: the sharks, rays, and chimaeras, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates.2,12 We reconstruct the sequence of reproductive mode evolution across a phylogeny of 610 chondrichthyans.13 We reveal egg laying as ancestral, with live bearing evolving at least seven times. Matrotrophy evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live bearing and matrotrophy are more prevalent in larger-bodied tropical species. Further, the evolution of live bearing is associated with a near doubling of the diversification rate, but there is only a small increase associated with the appearance of matrotrophy. Although pre-copulatory sexual selection is associated with increased rates of speciation in teleosts,3 sexual size dimorphism in chondrichthyans does not appear to be related to sexual selection,14,15 and instead we find increased rates of speciation associated with the colonization of novel habitats. This highlights a potential key difference between chondrichthyans and other fishes, specifically a slower rate of evolution of reproductive isolation following speciation, suggesting different rate-limiting mechanisms for diversification between these clades.16 The chondrichthyan diversification and radiation, particularly throughout shallow tropical shelf seas and oceanic pelagic habitats, appear to be associated with the evolution of live bearing and proliferation of a wide range of maternal investment in developing offspring.

Quantitative assessment of inner ear variation in elasmobranchs.

Considerable diversity has been documented in most sensory systems of elasmobranchs (sharks, rays, and skates); however, relatively little is known about morphological variation in the auditory system of these fishes. Using magnetic resonance imaging (MRI), the inner ear structures of 26 elasmobranchs were assessed in situ. The inner ear end organs (saccule, lagena, utricle, and macula neglecta), semi-circular canals (horizontal, anterior, and posterior), and endolymphatic duct were compared using phylogenetically-informed, multivariate analyses. Inner ear variation can be characterised by three primary axes that are influenced by diet and habitat, where piscivorous elasmobranchs have larger inner ears compared to non-piscivorous species, and reef-associated species have larger inner ears than oceanic species. Importantly, this variation may reflect differences in auditory specialisation that could be tied to the functional requirements and environmental soundscapes of different 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.

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade.

Understanding mating systems is a pillar of behavioural ecology, placing the complex interactions between females and males into a reproductive context. The field of multiple paternity, the phenomenon whereby many sires contribute to an individual litter, has traditionally viewed females as passive players in a male-male competitive framework. With the emergence of feminist perspectives in ecological fields, novel alternative mechanisms and evolutionary theories across invertebrate and vertebrate taxa recognize females are active stakeholders in the reproductive process. Despite their evolutionary significance, ecological diversity and myriad reproductive modes, elasmobranch (sharks, skates and rays) research lags behind other fields regarding complex biological processes, such as multiple paternity which is often ascribed to convenience polyandry. Here, we layout hypotheses and resynthesize multiple paternity literature from a female and life history perspective to highlight how alternative mechanisms influence the predominance of multiple paternity across elasmobranchs. We draw upon parallels in other invertebrate and vertebrate taxa to demonstrate how female elasmobranchs can influence multiple paternity outcomes that benefit their reproductive success. Our article challenges dogma that has resulted from years of dismissing the female perspective as important and provides a framework for future advancement using more holistic approaches to studying mating systems.

Maternal Investment, Ecological Lifestyle, and Brain Evolution in Sharks and Rays.

Across vertebrates increased maternal investment (via increased pre- and postnatal provisioning) is associated with larger relative brain size, yet it remains unclear how brain organization is shaped by life history and ecology. Here, we tested whether maternal investment and ecological lifestyle are related to variation in brain size and organization across 100 chondrichthyans. We hypothesized that brain size and organization would vary with the level of maternal investment and habitat depth and complexity. We found that chondrichthyan brain organization varies along four main axes according to (1) absolute brain size, (2) relative diencephalon and mesencephalon size, (3) relative telencephalon and medulla size, and (4) relative cerebellum size. Increased maternal investment is associated with larger relative brain size, while ecological lifestyle is informative for variation between relative telencephalon and medulla size and relative cerebellum size after accounting for the independent effects of reproductive mode. Deepwater chondrichthyans generally provide low levels of yolk-only (lecithotrophic) maternal investment and have relatively small brains, predominantly composed of medulla (a major portion of the hindbrain), whereas matrotrophic chondrichthyans-which provide maternal provisioning beyond the initial yolk sac-found in coastal, reef, or shallow oceanic habitats have relatively large brains, predominantly composed of telencephalon (a major portion of the forebrain). We have demonstrated, for the first time, that both ecological lifestyle and maternal investment are independently associated with brain organization in a lineage with diverse life-history strategies and reproductive modes.

Comparative Brain Morphology of the Greenland and Pacific Sleeper Sharks and its Functional Implications.

In cartilaginous fishes, variability in the size of the brain and its major regions is often associated with primary habitat and/or specific behavior patterns, which may allow for predictions on the relative importance of different sensory modalities. The Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic and are among the longest living vertebrates ever described. Despite a presumed visual impairment caused by the regular presence of parasitic ocular lesions, coupled with the fact that locomotory muscle power is often depressed at cold temperatures, these sharks remain capable of capturing active prey, including pinnipeds. Using magnetic resonance imaging (MRI), brain organization of S. microcephalus and S. pacificus was assessed in the context of up to 117 other cartilaginous fish species, using phylogenetic comparative techniques. Notably, the region of the brain responsible for motor control (cerebellum) is small and lacking foliation, a characteristic not yet described for any other large-bodied (>3 m) shark. Further, the development of the optic tectum is relatively reduced, while olfactory brain regions are among the largest of any shark species described to date, suggestive of an olfactory-mediated rather than a visually-mediated lifestyle.

Global priorities for conserving the evolutionary history of sharks, rays and chimaeras.

In an era of accelerated biodiversity loss and limited conservation resources, systematic prioritization of species and places is essential. In terrestrial vertebrates, evolutionary distinctness has been used to identify species and locations that embody the greatest share of evolutionary history. We estimate evolutionary distinctness for a large marine vertebrate radiation on a dated taxon-complete tree for all 1,192 chondrichthyan fishes (sharks, rays and chimaeras) by augmenting a new 610-species molecular phylogeny using taxonomic constraints. Chondrichthyans are by far the most evolutionarily distinct of all major radiations of jawed vertebrates-the average species embodies 26 million years of unique evolutionary history. With this metric, we identify 21 countries with the highest richness, endemism and evolutionary distinctness of threatened species as targets for conservation prioritization. On average, threatened chondrichthyans are more evolutionarily distinct-further motivating improved conservation, fisheries management and trade regulation to avoid significant pruning of the chondrichthyan tree of life.

An Introduction to Modelling Abundance and Life History Parameters in Shark Populations.

Elasmobranchs play critically important ecological roles throughout the world's oceans, yet in many cases, their slow life histories and interactions with fisheries makes them particularly susceptible to exploitation. Management for these species requires robust scientific input, and mathematical models are the backbone of science-based management. In this chapter, we provide an introductory overview of the use of mathematical models to estimate shark abundance. First, we discuss life history models that are used to understand the basic biology of elasmobranchs. Second, we cover population dynamics models, which are used to make inferences regarding population trend, size, and risk of extinction. Finally, we provide examples of applied models used to assess the status of elasmobranchs in the Northeast Pacific Ocean to guide management for these species. This chapter is not a comprehensive review of quantitative methods, but rather introduces various mathematical tools in fisheries management, with a focus on shark management in the Northeast Pacific Ocean.

Who's My Daddy? Considerations for the influence of sexual selection on multiple paternity in elasmobranch mating systems.

Polyandry resulting in multiply-sired litters has been documented in the majority of elasmobranch species examined to date. Although commonly observed, reasons for this mating system remain relatively obscure, especially in batoids. The round stingray (Urobatis halleri) is an abundant, well-studied elasmobranch distributed throughout the northeastern Pacific that we used to explore hypotheses regarding multiple paternity in elasmobranchs. Twenty mid- to late-term pregnant females were sampled off the coast of southern California and their litters analyzed for the occurrence of multiple paternity using five nuclear microsatellite loci. In addition, embryo sizes and their position within the female reproductive system (i.e., right or left uterus) were recorded and used to make inferences for patterns of ovulation. Multiple paternity was observed in 90% of litters and male reproductive success within litters was relatively even among sires. High variability in testes mass was observed suggesting that sperm competition is high in this species, although male reproductive success per litter appeared to be relatively even. Using embryo size as a proxy for fertilization, females were found to exhibit a variety of ovulation patterns that could function to limit a male's access to eggs and possibly promote high rates of multiple paternity. Our study highlights that elasmobranch mating systems may be more varied and complex than presumed and further investigation is warranted.

Evidence of maternal offloading of organic contaminants in white sharks (Carcharodon carcharias).

Organic contaminants were measured in young of the year (YOY) white sharks (Carcharodon carcharias) incidentally caught in southern California between 2005 and 2012 (n = 20) and were found to be unexpectedly high considering the young age and dietary preferences of young white sharks, suggesting these levels may be due to exposure in utero. To assess the potential contributions of dietary exposure to the observed levels, a five-parameter bioaccumulation model was used to estimate the total loads a newborn shark would potentially accumulate in one year from consuming contaminated prey from southern California. Maximum simulated dietary accumulation of DDTs and PCBs were 25.1 and 4.73 µg/g wet weight (ww) liver, respectively. Observed ΣDDT and ΣPCB concentrations (95±91 µg/g and 16±10 µg/g ww, respectively) in a majority of YOY sharks were substantially higher than the model predictions suggesting an additional source of contaminant exposure beyond foraging. Maternal offloading of organic contaminants during reproduction has been noted in other apex predators, but this is the first evidence of transfer in a matrotrophic shark. While there are signs of white shark population recovery in the eastern Pacific, the long-term physiological and population level consequences of biomagnification and maternal offloading of environmental contaminants in white sharks is unclear.

Heavy metal in children's tooth enamel: related to autism and disruptive behaviors?

To examine possible links between neurotoxicant exposure and neuropsychological disorders and child behavior, relative concentrations of lead, mercury, and manganese were examined in prenatal and postnatal enamel regions of deciduous teeth from children with Autism Spectrum Disorders (ASDs), high levels of disruptive behavior (HDB), and typically developing (TD) children. Using laser ablation inductively coupled plasma mass spectrometry, we found no significant differences in levels of these neurotoxicants for children with ASDs compared with TD children, but there was marginal significance indicating that children with ASDs have lower manganese levels. No significant differences emerged between children with HDB and TD children. The current findings challenge the notion that perinatal heavy metal exposure is a major contributor to the development of ASDs and HDB.

Seasonal reproduction of female round stingrays (Urobatis halleri): steroid hormone profiles and assessing reproductive state.

This study characterizes the seasonal reproductive cycle of female round stingrays (Urobatis halleri) in an open coastal site at Seal Beach, CA and a protected estuary at the Seal Beach National Wildlife Refuge (SBNWR). Female round stingrays were sampled from August 2004 to July 2006, and assessed for reproductive parameters (GSI, maximum ova diameter, pregnancy status) and sex steroid (estradiol (E(2)), progesterone (P(4)) and testosterone (T)) concentrations. E(2) and P(4) increased at the time of ovulation (June and July) and remained elevated until parturition (October and November); recently partruded females were observed until November. Mature females were absent from Seal Beach in August and September, the same time period that abundance of mature females peaked in the SBNWR. This aggregation of predominantly mature females in the upper reaches of the SBNWR was seasonal, and was observed from April to September. To better understand the aggregation behavior, sex steroid hormones were assayed in SBNWR females. In July and August, E(2) and P(4) concentrations in females at the SBNWR were 1.5-fold and 2-fold higher, respectively, than concentrations in mature females at Seal Beach, and correlated with elevated water temperature in the estuary. Pregnancy was confirmed in aggregating females by increased levels of E(2) and P(4) and the presence of developing embryos. Our data suggest that coastal estuaries may play a crucial role in round stingray reproduction, perhaps by providing a thermal refuge for pregnant females during gestation.

Photoperiod and water temperature regulation of seasonal reproduction in male round stingrays (Urobatis halleri).

This study characterizes the seasonal reproductive cycle of male round stingrays (Urobatis halleri) in Seal Beach, California. Mature round stingrays were collected monthly by beach seine near the San Gabriel River outfall from August 2004-September 2006, and rays were assessed for gametogenesis and steroid hormone levels. Male round stingrays exhibit a seasonal pattern of increased gonadosomatic index (GSI), spermatogenesis, and production of testosterone (T) and 11-ketotestosterone (11-KT). Based on GSI, the male reproductive cycle was broken into three distinct phases. TUNEL positive staining was only observed in the Sertoli cells of mature spermatocysts during the degenerative testicular phase, suggesting that Sertoli cell death potentially plays a role in testicular degeneration and the regulation of sperm release. GSI, T, and 11-KT were all inversely correlated with daylength, while only T was inversely correlated with temperature. Captive male round stingrays subjected to water temperatures of 25 degrees C showed a significant decrease in plasma testosterone concentrations, but the same males exposed to ambient water temperatures (18 degrees -20 degrees C) exhibited T concentrations observed in wild male round stingrays during the recrudescent phase. Together, these findings suggest that temperature plays an important role in the regulation of testosterone, and may serve as an ultimate cue for reproduction in male round stingrays.