Sarah L. Mesnick

Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).

The mechanisms that determine population structure in highly mobile marine species are poorly understood, but useful towards understanding the evolution of diversity, and essential for effective conservation and management. In this study, we compare putative sperm whale populations located in the Gulf of Mexico, western North Atlantic, Mediterranean Sea and North Sea using mtDNA control region sequence data and 16 polymorphic microsatellite loci. The Gulf of Mexico, western North Atlantic and North Sea populations each possessed similar low levels of haplotype and nucleotide diversity at the mtDNA locus, while the Mediterranean Sea population showed no detectable mtDNA diversity. Mitochondrial DNA results showed significant differentiation between all populations, while microsatellites showed significant differentiation only for comparisons with the Mediterranean Sea, and at a much lower level than seen for mtDNA. Samples from either side of the North Atlantic in coastal waters showed no differentiation for mtDNA, while North Atlantic samples from just outside the Gulf of Mexico (the western North Atlantic sample) were highly differentiated from samples within the Gulf at this locus. Our analyses indicate a previously unknown fidelity of females to coastal basins either side of the North Atlantic, and suggest the movement of males among these populations for breeding.

Interfamilial characterization of a region of the ZFX and ZFY genes facilitates sex determination in cetaceans and other mammals

Sequence polymorphism of homologues ZFX and ZFY, in a 604‐base pair exon region, was examined in 10 known males and 10 known females across seven cetacean families and used to design a simple, highly sensitive and widely applicable fluorescent 5′ exonuclease assay for gender determination in cetaceans. Multiplex amplification, cloning, and sequencing of these previously uncharacterized regions revealed (i) eight fixed differences between ZFX and ZFY, (ii) 29 variable sites between ZFX and ZFY and (iii) very low interspecific nucleotide diversity for both ZFX and ZFY across all families examined. We developed a 5′ exonuclease assay that produces a small (105 bp) polymerase chain reaction (PCR) product from both the X and the Y chromosome orthologs, and used double‐labelled fluorescent probes to distinguish between the two genes in a real‐time PCR assay that is highly reproducible and sensitive. We demonstrated sex specificity for 33 cetacean species in nine families. Given the availability of conserved primers and sequence information for many mammalian species, this approach to designing sexing assays for a wide range of species is both practical and efficient.

Sperm whale population structure in the eastern and central North Pacific inferred by the use of single-nucleotide polymorphisms, microsatellites and mitochondrial DNA.

We use mitochondrial DNA (mtDNA) (400 bp), six microsatellites and 36 single‐nucleotide polymorphisms (SNPs), 20 of which were linked, to investigate population structure of sperm whales (Physeter macrocephalus) in the eastern and central North Pacific. SNP markers, reproducible across technologies and laboratories, are ideal for long‐term studies of globally distributed species such as sperm whales, a species of conservation concern because of both historical and contemporary impacts. We estimate genetic differentiation among three strata in the temperate to tropical waters where females are found: California Current, Hawai`i and the eastern tropical Pacific. We then consider how males on sub‐Arctic foraging grounds assign to these strata. The California Current stratum was differentiated from both the other strata (P < 0.05) for mtDNA, microsatellites and SNPs, suggesting that the region supports a demographically independent population and providing the first indication that males may exhibit reproductive philopatry. Comparisons between the Hawai`i stratum and the eastern tropical Pacific stratum are not conclusive at this time. Comparisons with Alaska males were statistically significant, or nearly so, from all three strata and individuals showed mixed assignment to, and few exclusions from, the three potential source strata, suggesting widespread origin of males on sub‐Arctic feeding grounds. We show that SNPs have sufficient power to detect population structure even when genetic differentiation is low. There is a need for better analytical methods for SNPs, especially when linked SNPs are used, but SNPs appear to be a valuable marker for long‐term studies of globally dispersed and highly mobile species.

Normalization and binning of historical and multi-source microsatellite data: overcoming the problems of allele size shift with allelogram.

Microsatellite allele data have long been plagued by size shifts that can at best make it difficult to accurately assign genotypes to allele products, and at worse can cause whole batches of data from different instruments, dates or laboratories to be incorrectly assigned. Although modern genotyping technology (capillary electrophoresis) has overcome many of these problems, concern remains regarding the consistency of scores within a laboratory over time and between laboratories when combining data from multiple sources into a single analysis. There remain a large number of laboratories using older technologies or combining data from multiple sources. In addition, thousands of data sets that could potentially be expanded as samples become available are generally regarded as unusable because of the effort that would be required to validate congruence of genotypes from old and new data sets. We present methods to normalize and bin alleles from multiple data sources using a relatively small set of controls and the freely available program allelogram.

Social and Behavioural Factors in Cetacean Responses to Overexploitation: Are Odontocetes Less “Resilient” Than Mysticetes?

Many severely depleted populations of baleen whales (Mysticeti) have exhibited clear signs of recovery whereas there are few examples in toothed whales (Odontoceti). We hypothesize that this difference is due, at least in part, to social and behavioural factors. Clearly, a part of the lack of resilience to exploitation is explained by odontocete life history. However, an additional factor may be the highly social nature of many odontocetes in which survival and reproductive success may depend on: (a) social cohesion and organization, (b) mutual defence against predators and possible alloparental care, (c) inter-generational transfer of “knowledge”, and (d) leadership by older individuals. We found little evidence of strong recovery in any of the depleted populations examined. Their relatively low potential rates of increase mean that odontocete populations can be over-exploited with take rates of only a few percent per year. Exploitation can have effects beyond the dynamics of individual removals. Four species showed evidence of a decrease in birth rates following exploitation; potential mechanisms include a deficit of adult females, a deficit of adult males, and disruption of mating systems. The evidence for a lack of strong recovery in heavily exploited odontocete populations indicates that management should be more precautionary.

A trade-off between precopulatory and postcopulatory trait investment in male cetaceans

Mating with multiple partners is common across species, and understanding how individual males secure fertilization in the face of competition remains a fundamental goal of evolutionary biology. Game theory stipulates that males have a fixed budget for reproduction that can lead to a trade‐off between investment in precopulatory traits such as body size, armaments, and ornaments, and postcopulatory traits such as testis size and spermatogenic efficiency. Recent theoretical and empirical studies have shown that if males can monopolize access to multiple females, they will invest disproportionately in precopulatory traits and less in postcopulatory traits. Using phylogenetically controlled comparative methods, we demonstrate that across 58 cetacean species with the most prominent sexual dimorphism in size, shape, teeth, tusks, and singing invest significantly less in relative testes mass. In support of theoretical predictions, these species tend to show evidence of male contests, suggesting there is opportunity for winners to monopolize access to multiple females. Our approach provides a robust dataset with which to make predictions about male mating strategies for the many cetacean species for which adequate behavioral observations do not exist.

What influences the worldwide genetic structure of sperm whales (Physeter macrocephalus)

The interplay of natural selection and genetic drift, influenced by geographic isolation, mating systems and population size, determines patterns of genetic diversity within species. The sperm whale provides an interesting example of a long‐lived species with few geographic barriers to dispersal. Worldwide mtDNA diversity is relatively low, but highly structured among geographic regions and social groups, attributed to female philopatry. However, it is unclear whether this female philopatry is due to geographic regions or social groups, or how this might vary on a worldwide scale. To answer these questions, we combined mtDNA information for 1091 previously published samples with 542 newly obtained DNA profiles (394‐bp mtDNA, sex, 13 microsatellites) including the previously unsampled Indian Ocean, and social group information for 541 individuals. We found low mtDNA diversity (π = 0.430%) reflecting an expansion event <80 000 years bp, but strong differentiation by ocean, among regions within some oceans, and among social groups. In comparison, microsatellite differentiation was low at all levels, presumably due to male‐mediated gene flow. A hierarchical amova showed that regions were important for explaining mtDNA variance in the Indian Ocean, but not Pacific, with social group sampling in the Atlantic too limited to include in analyses. Social groups were important in partitioning mtDNA and microsatellite variance within both oceans. Therefore, both geographic philopatry and social philopatry influence genetic structure in the sperm whale, but their relative importance differs by sex and ocean, reflecting breeding behaviour, geographic features and perhaps a more recent origin of sperm whales in the Pacific. By investigating the interplay of evolutionary forces operating at different temporal and geographic scales, we show that sperm whales are perhaps a unique example of a worldwide population expansion followed by rapid assortment due to female social organization.

Pacific Ocean–Wide Profile of CYP1A1 Expression, Stable Carbon and Nitrogen Isotope Ratios, and Organic Contaminant Burden in Sperm Whale Skin Biopsies

Background Ocean pollution affects marine organisms and ecosystems as well as humans. The International Oceanographic Commission recommends ocean health monitoring programs to investigate the presence of marine contaminants and the health of threatened species and the use of multiple and early-warning biomarker approaches. Objective We explored the hypothesis that biomarker and contaminant analyses in skin biopsies of the threatened sperm whale (Physeter macrocephalus) could reveal geographical trends in exposure on an oceanwide scale. Methods We analyzed cytochrome P450 1A1 (CYP1A1) expression (by immunohistochemistry), stable nitrogen and carbon isotope ratios (as general indicators of trophic position and latitude, respectively), and contaminant burdens in skin biopsies to explore regional trends in the Pacific Ocean. Results Biomarker analyses revealed significant regional differences within the Pacific Ocean. CYP1A1 expression was highest in whales from the Galapagos, a United Nations Educational, Scientific, and Cultural Organization World Heritage marine reserve, and was lowest in the sampling sites farthest away from continents. We examined the possible influence of the whales’ sex, diet, or range and other parameters on regional variation in CYP1A1 expression, but data were inconclusive. In general, CYP1A1 expression was not significantly correlated with contaminant burdens in blubber. However, small sample sizes precluded detailed chemical analyses, and power to detect significant associations was limited. Conclusions Our large-scale monitoring study was successful at identifying regional differences in CYP1A1 expression, providing a baseline for this known biomarker of exposure to aryl hydrocarbon receptor agonists. However, we could not identify factors that explained this variation. Future oceanwide CYP1A1 expression profiles in cetacean skin biopsies are warranted and could reveal whether globally distributed chemicals occur at biochemically relevant concentrations on a global basis, which may provide a measure of ocean integrity.

Research Priorities from Animal Behaviour for Maximising Conservation Progress

Poor communication between academic researchers and wildlife managers limits conservation progress and innovation. As a result, input from overlapping fields, such as animal behaviour, is underused in conservation management despite its demonstrated utility as a conservation tool and countless papers advocating its use. Communication and collaboration across these two disciplines are unlikely to improve without clearly identified management needs and demonstrable impacts of behavioural-based conservation management. To facilitate this process, a team of wildlife managers and animal behaviour researchers conducted a research prioritisation exercise, identifying 50 key questions that have great potential to resolve critical conservation and management problems. The resulting agenda highlights the diversity and extent of advances that both fields could achieve through collaboration.

A systematic survey of the integration of animal behavior into conservation

The role of behavioral ecology in improving wildlife conservation and management has been the subject of much recent debate. We sought to answer 2 foundational questions about the current use of behavioral knowledge in conservation: To what extent is behavioral knowledge used in wildlife conservation and management, and how does the use of animal behavior differ among conservation fields in both frequency and types of use? We searched the literature for intersections between key fields of animal behavior and conservation and created a systematic heat map (i.e., graphical representation of data where values are represented as colors) to visualize relative efforts. Some behaviors, such as dispersal and foraging, were commonly considered (mean [SE] of 1147.38 [353.11] and 439.44 [108.85] papers per cell, respectively). In contrast, other behaviors, such as learning, social, and antipredatory behaviors were rarely considered (mean [SE] of 33.88 [7.62], 44.81 [10.65], and 22.69 [6.37] papers per cell, respectively). In many cases, awareness of the importance of behavior did not translate into applicable management tools. Our results challenge previous suggestions that there is little association between the fields of behavioral ecology and conservation and reveals tremendous variation in the use of different behaviors in conservation. We recommend that researchers focus on examining underutilized intersections of behavior and conservation themes for which preliminary work shows a potential for improving conservation and management, translating behavioral theory into applicable and testable predictions, and creating systematic reviews to summarize the behavioral evidence within the behavior-conservation intersections for which many studies exist.