Tal Ben-Horin

Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.

We combine kinship estimates with traditional F‐statistics to explain contemporary drivers of population genetic differentiation despite high gene flow. We investigate range‐wide population genetic structure of the California spiny (or red rock) lobster (Panulirus interruptus) and find slight, but significant global population differentiation in mtDNA (ΦST = 0.006, P = 0.001; Dest_Chao = 0.025) and seven nuclear microsatellites (FST = 0.004, P < 0.001; Dest_Chao = 0.03), despite the species’ 240‐ to 330‐day pelagic larval duration. Significant population structure does not correlate with distance between sampling locations, and pairwise FST between adjacent sites often exceeds that among geographically distant locations. This result would typically be interpreted as unexplainable, chaotic genetic patchiness. However, kinship levels differ significantly among sites (pseudo‐F16,988 = 1.39, P = 0.001), and ten of 17 sample sites have significantly greater numbers of kin than expected by chance (P < 0.05). Moreover, a higher proportion of kin within sites strongly correlates with greater genetic differentiation among sites (Dest_Chao, R2 = 0.66, P < 0.005). Sites with elevated mean kinship were geographically proximate to regions of high upwelling intensity (R2 = 0.41, P = 0.0009). These results indicate that P. interruptus does not maintain a single homogenous population, despite extreme dispersal potential. Instead, these lobsters appear to either have substantial localized recruitment or maintain planktonic larval cohesiveness whereby siblings more likely settle together than disperse across sites. More broadly, our results contribute to a growing number of studies showing that low FST and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.

Mapping Physiological Suitability Limits for Malaria in Africa Under Climate Change

Abstract We mapped current and future temperature suitability for malaria transmission in Africa using a published model that incorporates nonlinear physiological responses to temperature of the mosquito vector Anopheles gambiae and the malaria parasite Plasmodium falciparum. We found that a larger area of Africa currently experiences the ideal temperature for transmission than previously supposed. Under future climate projections, we predicted a modest increase in the overall area suitable for malaria transmission, but a net decrease in the most suitable area. Combined with human population density projections, our maps suggest that areas with temperatures suitable for year-round, highest-risk transmission will shift from coastal West Africa to the Albertine Rift between the Democratic Republic of Congo and Uganda, whereas areas with seasonal transmission suitability will shift toward sub-Saharan coastal areas. Mapping temperature suitability places important bounds on malaria transmissibility and, along with local level demographic, socioeconomic, and ecological factors, can indicate where resources may be best spent on malaria control.

Variable intertidal temperature explains why disease endangers black abalone

Epidemiological theory suggests that pathogens will not cause host extinctions because agents of disease should fade out when the host population is driven below a threshold density. Nevertheless, infectious diseases have threatened species with extinction on local scales by maintaining high incidence and the ability to spread efficiently even as host populations decline. Intertidal black abalone (Haliotis cracherodii), but not other abalone species, went extinct locally throughout much of southern California following the emergence of a Rickettsiales-like pathogen in the mid-1980s. The rickettsial disease, a condition known as withering syndrome (WS), and associated mortality occur at elevated water temperatures. We measured abalone body temperatures in the field and experimentally manipulated intertidal environmental conditions in the laboratory, testing the influence of mean temperature and daily temperature variability on key epizootiological processes of WS. Daily temperature variability increased the susceptibility of black abalone to infection, but disease expression occurred only at warm water temperatures and was independent of temperature variability. These results imply that high thermal variation of the marine intertidal zone allows the pathogen to readily infect black abalone, but infected individuals remain asymptomatic until water temperatures periodically exceed thresholds modulating WS. Mass mortalities can therefore occur before pathogen transmission is limited by density-dependent factors.

Utilizing spatial demographic and life history variation to optimize sustainable yield of a temperate sex-changing fish.

Fish populations vary geographically in demography and life history due to environmental and ecological processes and in response to exploitation. However, population dynamic models and stock assessments, used to manage fisheries, rarely explicitly incorporate spatial variation to inform management decisions. Here, we describe extensive geographic variation in several demographic and life history characteristics (e.g., size structure, growth, survivorship, maturation, and sex change) of California sheephead (Semicossyphus pulcher), a temperate rocky reef fish targeted by recreational and commercial fisheries. Fish were sampled from nine locations throughout southern California in 2007–2008. We developed a dynamic size and age-structured model, parameterized separately for each location, to assess the potential cost or benefit in terms of fisheries yield and conservation objectives of changing minimum size limits and/or fishing mortality rates (compared to the status quo). Results indicate that managing populations individually, with location-specific regulations, could increase yield by over 26% while maintaining conservative levels of spawning biomass. While this local management approach would be challenging to implement in practice, we found statistically similar increases in yield could be achieved by dividing southern California into two separate management regions, reflecting geographic similarities in demography. To maximize yield, size limits should be increased by 90 mm in the northern region and held at current levels in the south. We also found that managing the fishery as one single stock (the status quo), but with a size limit 50 mm greater than the current regulations, could increase overall fishery yield by 15%. Increases in size limits are predicted to enhance fishery yield and may also have important ecological consequences for the predatory role of sheephead in kelp forests. This framework for incorporating demographic variation into fisheries models can be exported generally to other species and may aid in identifying the appropriate spatial scales for fisheries management.

Understanding uncertainty in temperature effects on vector-borne disease: a Bayesian approach

Extrinsic environmental factors influence the distribution and population dynamics of many organisms, including insects that are of concern for human health and agriculture. This is particularly true for vector-borne infectious diseases like malaria, which is a major source of morbidity and mortality in humans. Understanding the mechanistic links between environment and population processes for these diseases is key to predicting the consequences of climate change on transmission and for developing effective interventions. An important measure of the intensity of disease transmission is the reproductive number R0. However, understanding the mechanisms linking R0 and temperature, an environmental factor driving disease risk, can be challenging because the data available for parameterization are often poor. To address this, we show how a Bayesian approach can help identify critical uncertainties in components of R0 and how this uncertainty is propagated into the estimate of R0. Most notably, we find that different parameters dominate the uncertainty at different temperature regimes: bite rate from 15 degrees C to 25 degrees C; fecundity across all temperatures, but especially approximately 25-32 degrees C; mortality from 20 degrees C to 30 degrees C; parasite development rate at degrees 15-16 degrees C and again at approximately 33-35 degrees C. Focusing empirical studies on these parameters and corresponding temperature ranges would be the most efficient way to improve estimates of R0. While we focus on malaria, our methods apply to improving process-based models more generally, including epidemiological, physiological niche, and species distribution models.

Parasite transmission through suspension feeding.

Suspension-feeding bivalve molluscs are confronted with a wide range of materials in the benthic marine environment. These materials include various sized plankton and the organic material derived from it, macroalgae, detritus and a diversity of microbial parasites that have adapted life stages to survive in the water column. For bivalve parasites to infect hosts though, they must first survive and remain infectious in the water column to make initial contact with hosts, and once in contact, enter and overcome elaborate pathways for particle sorting and selection. Even past these defenses, bivalve parasites are challenged with efficient systems of mechanical and chemical digestion and highly evolved systems of innate immunity. Here we review how bivalve parasites evade these hurdles to complete their life cycles and establish within bivalve hosts. We broadly cover significant viral, bacterial, and protozoan parasites of marine bivalve molluscs, and illustrate the emergent properties of these host-parasite systems where parasite transmission occurs through suspension feeding.

Fishing diseased abalone to promote yield and conservation

Past theoretical models suggest fishing disease-impacted stocks can reduce parasite transmission, but this is a good management strategy only when the exploitation required to reduce transmission does not overfish the stock. We applied this concept to a red abalone fishery so impacted by an infectious disease (withering syndrome) that stock densities plummeted and managers closed the fishery. In addition to the non-selective fishing strategy considered by past disease-fishing models, we modelled targeting (culling) infected individuals, which is plausible in red abalone because modern diagnostic tools can determine infection without harming landed abalone and the diagnostic cost is minor relative to the catch value. The non-selective abalone fishing required to eradicate parasites exceeded thresholds for abalone sustainability, but targeting infected abalone allowed the fishery to generate yield and reduce parasite prevalence while maintaining stock densities at or above the densities attainable if the population was closed to fishing. The effect was strong enough that stock and yield increased even when the catch was one-third uninfected abalone. These results could apply to other fisheries as the diagnostic costs decline relative to catch value.

Characterization of eight polymorphic microsatellite loci for the California spiny lobster, Panulirus interruptus and cross-amplification in other achelate lobsters

Microsatellite sequences were isolated from both non-enriched and enriched genomic libraries of California spiny lobster, Panulirus interruptus. Eight consistently amplifying, scorable and polymorphic loci were characterized for 79 individuals collected at Santa Cruz and San Clemente Islands, California, and tested for cross-species amplification in four closely related Panulirus spp., as well as four other species of the order Achelata. The number of alleles observed per locus ranged from three to 54 and observed heterozygosities ranged from 0.57 to 0.98. Quality control testing shows that all loci were reliably scorable, independently segregating, inherited in Mendelian ratios, and had low to moderate (≤14.4%) frequencies of null alleles and high statistical power for detecting fine scale genetic structure.

Abalone farm discharges the withering syndrome pathogen into the wild

An intracellular bacterium Candidatus Xenohaliotis californiensis, also called Withering-Syndrome Rickettsia-Like Organism (WS-RLO), is the cause of mass mortalities that are the chief reason for endangerment of black abalone (Haliotis cracherodii). Using a real-time PCR assay, we found that a shore-based abalone farm (AF) in Santa Barbara, CA, USA discharged WS-RLO DNA into the ocean. Several other shore-based AFs discharge effluent into critical habitat for black abalone in California and this might affect the recovery of wild black abalone. Existing regulatory frameworks exist that could help protect wild species from pathogens released from shore-based aquaculture.

Malaria control and senescence: the importance of accounting for the pace and shape of aging in wild mosquitoes

The assumption that vector mortality remains constant with age is used widely to assess malaria transmission risk and predict the public health consequences of vector control strategies. However, laboratory studies commonly demonstrate clear evidence of senescence, or a decrease in physiological function and increase in vector mortality rate with age. Despite recognition of its importance, practical limitations have stifled definitive observations of mosquito senescence in the wild, where rates of extrinsic mortality are much higher than those observed under protected laboratory conditions. We developed methods to integrate available field data to understand mortality in wild Anopheles gambiae, the most import vector of malaria in sub-Saharan Africa. We found evidence for an increase in rates of mortality with age. As expected, we also found that overall mortality is far greater in wild cohorts than commonly observed under protected laboratory conditions. The magnitude of senescence increases with An. gambiae lifespan, implying that most wild mosquitoes die long before cohorts can exhibit strong senescence. We reviewed available published mortality studies of Anopheles spp. to confirm this fundamental prediction of aging in wild populations. Senescence becomes most apparent in long-living mosquito cohorts; cohorts with low extrinsic mortality, such as protected laboratory cohorts, suffer a relatively high proportion of senescent deaths. Imprecision in estimates of vector mortality and changes in mortality with age will severely bias models of vector borne disease transmission risk, such as malaria, and the sensitivity of transmission to bias increases as the extrinsic incubation period of the parasite decreases. While we focus here on malaria, we caution that future transmission models of anti-vectorial interventions must incorporate both realistic mortality rates and age-dependent changes in mortality.