Mixed population genomics support for the central marginal hypothesis across the invasive range of the cane toad (Rhinella marina) in Australia

Understanding factors that cause species' geographic range limits is a major focus in ecology and evolution. The central marginal hypothesis (CMH) predicts that species cannot adapt to conditions beyond current geographic range edges because genetic diversity decreases from core to edge due to smaller, more isolated edge populations. We employed a population genomics framework using 24 235–33 112 SNP loci to test major predictions of the CMH in the ongoing invasion of the cane toad (Rhinella marina) in Australia. Cane toad tissue samples were collected along broad‐scale, core‐to‐edge transects across their invasive range. Geographic and ecological core areas were identified using GIS and habitat suitability indices from ecological niche modelling. Bayesian clustering analyses revealed three genetic clusters, in the northwest invasion‐front region, northeast precipitation‐limited region and southeast cold temperature‐limited region. Core‐to‐edge patterns of genetic diversity and differentiation were consistent with the CMH in the southeast, but were not supported in the northeast and showed mixed support in the northwest. Results suggest cold temperatures are a likely contributor to southeastern range limits, consistent with CMH predictions. In the northeast and northwest, ecological processes consisting of a steep physiological barrier and ongoing invasion dynamics, respectively, are more likely explanations for population genomic patterns than the CMH.     

Nutrition, hormones and life history in burying beetles

Nutrition, hormones and the allocation of physiological resources are intricately related. To investigate these inter-relationships in female burying beetles (Nicrophorus spp.), we examined the effect of diet quality on juvenile hormone (JH) levels and reproduction, and the effect of JH supplementation on reproduction and resistance to starvation. Nicrophorus orbicollis adult females fed a less preferred mealworm larvae diet gained less body mass, had smaller ovaries and had lower titers of JH in their hemolymph than females fed a preferred blowfly diet. When presented a carcass for breeding, females on a less preferred diet oviposited 33% fewer eggs, and eggs were of 18% less mass. Females on the less preferred diet also took longer to begin oviposition as indicated indirectly by the time when their eggs hatched. To investigate the effects of JH, independent of nutrition, JH was topically applied to single and paired females of Nicrophorus tomentosus. When presented a carcass, JH-treated paired females oviposited more eggs (28%-year 1, 44%-year 2) than control females, and also showed a trend toward faster oviposition. JH supplementation had a greater effect on single females. JH treatment increased the proportion of single females attempting reproduction (at least one viable larva), increased the number of eggs (69%-year 1, 123%-year 2), and increased the proportion of females ovipositing early. In separate experiments, treatment with JH or a JH analog negatively affected resistance to starvation in three species. Treatment with JH reduced starvation survival by 10.3% days in N. tomentosus females. Treatment with the JH analog methoprene reduced starvation survival 17.8% in N. orbicollis females and by 18% in Ptomascopus morio females. These results suggest that JH has positive and negative effects on different components of life history.     

Social and nonsocial stimuli and juvenile hormone titer in a male burying beetle, Nicrophorus orbicollis

We investigated the interaction of social and nonsocial stimuli on juvenile hormone (JH) titer in male burying beetles (Nicrophorus orbicollis). The initial JH response to discovery of a carcass was substantial (10-15-fold increase over controls) and rapid (<1h), and occurred whether or not a female was present. By 3h after discovery, JH titers were declining, the decline being more pronounced when a female was not present. We also tested the effect of larval stimulation on JH titer in care-giving males by removing a male's brood and replacing it with a brood of first or third instar larvae. Males initially providing care for begging first instar larvae continued to maintain high titers of JH when the replacement broods were first but not third instars. Males caring for third instar larvae (normally low JH titers) maintained low levels of JH regardless of the developmental stage of the replacement brood. This suggests that once males begin to care for nutritionally independent third instar larvae, JH titers remain low regardless of subsequent larval stimulation. Burying beetles are socially and hormonally complex organisms in which stimuli from a breeding resource, mating partners, rivals and young interact to alter the JH profile of breeding adults.     

Urban landscapes can change virus gene flow and evolution in a fragmentation‐sensitive carnivore

Urban expansion has widespread impacts on wildlife species globally, including the transmission and emergence of infectious diseases. However, there is almost no information about how urban landscapes shape transmission dynamics in wildlife. Using an innovative phylodynamic approach combining host and pathogen molecular data with landscape characteristics and host traits, we untangle the complex factors that drive transmission networks of feline immunodeficiency virus (FIV) in bobcats (Lynx rufus). We found that the urban landscape played a significant role in shaping FIV transmission. Even though bobcats were often trapped within the urban matrix, FIV transmission events were more likely to occur in areas with more natural habitat elements. Urban fragmentation also resulted in lower rates of pathogen evolution, possibly owing to a narrower range of host genotypes in the fragmented area. Combined, our findings show that urban landscapes can have impacts on a pathogen and its evolution in a carnivore living in one of the most fragmented and urban systems in North America. The analytical approach used here can be broadly applied to other host–pathogen systems, including humans.     

Molecular systematics and biogeography of Nicrophorus in part--the investigator species group (Coleoptera: Silphidae) using mixture model MCMC

Burying beetles (Silphidae: Nicrophorus) are well-known for their biparental care and monopolization of small vertebrate carcasses in subterranean crypts. They have been the focus of intense behavioral ecological research since the 1980s yet no thorough phylogenetic estimate for the group exists. The relationships among the species, and the validity of some species, are poorly understood. Here, we infer the relationships and examine species boundaries among 50 individuals representing 15 species, primarily of the investigator species group, using a mixture-model Bayesian analysis. Two mitochondrial genes, COI and COII, were used, providing 2129 aligned nucleotides (567 parsimony-informative). The Akaike Information Criterion and Bayes Factors were used to select the best fitting model, in addition to Reversible Jump MCMC, which accommodated model uncertainty. A 21 parameter, three-partition GTR + G was the final model chosen. Despite a presumed Old World origin for the genus itself, the basal lineages and immediate outgroups of the investigator species group are New World species. Bayesian methods reconstruct the common ancestor of the investigator species group as New World and imply one later transition to the Old World with two return transitions to the New World. Prior hypotheses concerning the questionable validity of four species names, Nicrophorus praedator, Nicrophorus confusus, Nicrophorus encaustus and Nicrophorus mexicanus were tested. No evidence was found for the validity of the Nicrophorus investigator synonym N. praedator. We found evidence rejecting the species status of N. confusus (NEW SYNONYM of Nicrophorus sepultor). Weak evidence was found for the species status of N. encaustus and N. mexicanus, which are tentatively retained as valid. Our results strongly reject a recently published hypothesis that Nicrophorus interruptus (NEW STATUS as valid species) is a subspecies of N. investigator.     

Changes in biosynthesis and degradation of juvenile hormone during breeding by burying beetles: a reproductive or social role?

Burying beetles, Nicrophorus orbicollis, depend on the location of an unpredictable resource, a small vertebrate carcass, for reproduction. When they discover a carcass, they undergo a correlated rapid rise in titers of juvenile hormone (JH) in the hemolymph and ovarian development. This study investigates the regulation of the changes in JH during breeding in both male and female burying beetles and the role of JH in ovarian development. JH biosynthesis by the corpora allata (CA), measured in vitro, increased in females within an hour of their discovery of a carcass and increased later in males. After returning to low rates as oviposition began, JH biosynthesis rose again 3 days later in females but not in males. Neither the ovaries nor testes synthesized JH. There was a concomitant fall in JH esterase activity within 12 h of discovery of the carcass in both males and females. Although the rise in JH titers and biosynthesis and the fall in JH esterase is correlated with ovarian development, application of methoprene or JH III in the absence of a carcass did not result in vitellogenin uptake by the oocytes. Therefore, we conclude that, in spite of the rapid rise in JH before oviposition, it is not sufficient to regulate vitellogenin synthesis and/or its uptake by the ovaries. We suggest that its role has been preempted to organize social behavior and coordinate parental behavior between mates.     

Habitat Fragmentation and Burying Beetle Abundance and Success

Four species of burying beetle (Nicrophorus marginatus F., N. tomentosus Weber, N. orbicollis Say and N. defodiens Mannerheim) are attracted to small, fresh mouse carcasses in northern Michigan. The number of burying beetles and their success (burial of a carcass) were greater in woodlands than in edge or field habitats. Species diversity was least in open fields as assessed by two different indices of diversity. Nicrophorus marginatus was the only species captured in large fields (<25ha). This species was never trapped in small fields (>5ha) suggesting that a minimum habitat size might be necessary to maintain local populations. In contrast to previous studies which employed pitfall traps baited with a large quantity of carrion, N. tomentosus was caught exclusively in woodlands at single mouse carcasses. In Connecticut woodlands, burying beetle success, assayed as the proportion of carcasses buried and held for 7 days, was significantly greater in larger as compared to smaller woodlands. The limited success of burying beetles in smaller woodlands was due, in part, to a higher rate of scavenging by vertebrates.     

Urbanization impacts apex predator gene flow but not genetic diversity across an urban‐rural divide

Apex predators are important indicators of intact natural ecosystems. They are also sensitive to urbanization because they require broad home ranges and extensive contiguous habitat to support their prey base. Pumas (Puma concolor) can persist near human developed areas, but urbanization may be detrimental to their movement ecology, population structure, and genetic diversity. To investigate potential effects of urbanization in population connectivity of pumas, we performed a landscape genomics study of 130 pumas on the rural Western Slope and more urbanized Front Range of Colorado, USA. Over 12,000 single nucleotide polymorphisms (SNPs) were genotyped using double‐digest, restriction site‐associated DNA sequencing (ddRADseq). We investigated patterns of gene flow and genetic diversity, and tested for correlations between key landscape variables and genetic distance to assess the effects of urbanization and other landscape factors on gene flow. Levels of genetic diversity were similar for the Western Slope and Front Range, but effective population sizes were smaller, genetic distances were higher, and there was more admixture in the more urbanized Front Range. Forest cover was strongly positively associated with puma gene flow on the Western Slope, while impervious surfaces restricted gene flow and more open, natural habitats enhanced gene flow on the Front Range. Landscape genomic analyses revealed differences in puma movement and gene flow patterns in rural versus urban settings. Our results highlight the utility of dense, genome‐scale markers to document subtle impacts of urbanization on a wide‐ranging carnivore living near a large urban center.     

Conservation genetics of an island-endemic lizard: low Ne and the critical role of intermediate temperatures for genetic connectivity

Island populations are at higher risk of extinction than mainland populations. Therefore, understanding the factors that facilitate connectivity is particularly pressing for the conservation of island taxa. Sceloporus occidentalis becki, the Island Fence Lizard, is an endemic taxon restricted to the Northern Channel Islands, part of a nearshore archipelago in Southern California, USA. Since the Last Glacial Maximum, fence lizard habitat on the Northern Channel Islands has decreased with rising sea levels and increasing temperatures that have reduced the availability of woody vegetation. More recently, the introduction (and subsequent removal) of invasive ungulates over the last 170 years and recovery of vegetation has resulted in further dramatic habitat modification. Given the potential for genetic bottlenecks, the history of habitat alteration, and topographic and landscape complexity, we used landscape and population genetic approaches to characterize patterns of genetic diversity and structure of Island Fence Lizards on Santa Cruz Island, the largest of the Northern Channel Islands. Our analyses revealed shallow population structure across the island, low effective population size (N_e?=??~?200), and evidence for a recent genetic bottleneck. Landscape genetic analyses showed that connectivity is facilitated by tree canopy cover and shrubland, as well as by intermediate temperatures, emphasizing the importance of woody vegetation and habitats with variable thermal regimes as the climate warms. Combined, these population and landscape genetic analyses suggest that the Island Fence Lizard is of greater conservation concern than currently appreciated, and increased conservation management focus is warranted for this island endemic.