Michael F. Antolin

Ecological neighborhoods: scaling environmental patterns

In this paper we review, develop, and differentiate among concepts associated with environmental patterning (patch, division, and heterogeneity), spatial and temporal scales of ecological processes (ecological neighborhoods), and responses of organisms to environmental patterning (relative patch size, relative patch duration, relative patch isolation, and grain response). We generalize the concept of ecological neighborhoods to represent regions of activity or influence during periods of time appropriate to particular ecological processes. Therefore, there is no single ecological neighborhood for any given organism, but rather a number of neighborhoods, each appropriate to different processes. Neighborhood sizes can be estimated by examining the cumulative distribution of activity or influence of an organism as a function of increasingly large spatial units. The spatial and temporal dimensions of neighborhoods provide the scales necessary for assessing environmental patterning relative to particular ecological processes for a given species. Consistent application of the neighborhood concept will assist in the choice of appropriate study units, comparisons among different studies, and comparisons between empirical studies and theoretical postulates.

Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics

Plague is a highly virulent disease believed to have killed millions during three historic human pandemics. Worldwide, it remains a threat to humans and is a potential agent of bioterrorism. Dissemination of Yersinia pestis, the etiological agent of plague, by blocked fleas has been the accepted paradigm for flea-borne transmission. However, this mechanism, which requires a lengthy extrinsic incubation period before a short infectious window often followed by death of the flea, cannot sufficiently explain the rapid rate of spread that typifies plague epidemics and epizootics. Inconsistencies between the expected rate of spread by blocked rat fleas and that observed during the Black Death has even caused speculation that plague was not the cause of this medieval pandemic. We used the primary vector to humans in North America, Oropsylla montana, which rarely becomes blocked, as a model for studying alternative flea-borne transmission mechanisms. Our data revealed that, in contrast to the classical blocked flea model, O. montana is immediately infectious, transmits efficiently for at least 4 d postinfection (early phase) and may remain infectious for a long time because the fleas do not suffer block-induced mortality. These factors match the criteria required to drive plague epizootics as defined by recently published mathematical models. The scenario of efficient early-phase transmission by unblocked fleas described in our study calls for a paradigm shift in concepts of how Y. pestis is transmitted during rapidly spreading epizootics and epidemics, including, perhaps, the Black Death.

Finding the genomic basis of local adaptation: Pitfalls, practical solutions, and future directions

Uncovering the genetic and evolutionary basis of local adaptation is a major focus of evolutionary biology. The recent development of cost-effective methods for obtaining high-quality genome-scale data makes it possible to identify some of the loci responsible for adaptive differences among populations. Two basic approaches for identifying putatively locally adaptive loci have been developed and are broadly used: one that identifies loci with unusually high genetic differentiation among populations (differentiation outlier methods) and one that searches for correlations between local population allele frequencies and local environments (genetic-environment association methods). Here, we review the promises and challenges of these genome scan methods, including correcting for the confounding influence of a species’ demographic history, biases caused by missing aspects of the genome, matching scales of environmental data with population structure, and other statistical considerations. In each case, we make suggestions for best practices for maximizing the accuracy and efficiency of genome scans to detect the underlying genetic basis of local adaptation. With attention to their current limitations, genome scan methods can be an important tool in finding the genetic basis of adaptive evolutionary change.

Brood-mate avoidance in the parasitic waspBracon hebetorSay

The parasitic waspBracon hebetorsuffers severe inbreeding depression. This study examined two behavioural mechanisms that minimize mating between close relatives. First, the majority of males and females were unwilling to mate immediately upon emergence. Receptivity to mating slowly increased with age of the adult. By the time most individuals were willing to mate, the majority of wasps had dispersed from the natal site. Second, females tended to avoid mating with brood-mates when given a choice between a male that developed on the same host and one that developed on a different host. Experiments using eye-colour mutants and broods composed of relatives and non-relatives indicated that females discriminated against male brood-mates on the basis of environmental cues. Females consistently mated with brothers and non-brothers if they developed on another host, but tended to reject brothers and non-brothers from the same brood as themselves. Females maintained the ability to recognize brood-mates for at least 5 days after eclosion.

A genetic perspective on mating systems and sex ratios of parasitoid wasps

Parasitoid sex ratios are influenced by mating systems, whether complete inbreeding, partial inbreeding, complete inbreeding avoidance, or production of all-male broods by unmated females. Population genetic theory demonstrates that inbreeding is possible in haplodiploids because the purging of deleterious and lethal mutations through haploid males reduces inbreeding depression. However, this purging does not act quickly for deleterious mutations or female-limited traits (e.g., fecundity, host searching, sex ratio). The relationship between sex ratio, inbreeding, and inbreeding depression has not been explored in depth in parasitoids. The gregarious egg parasitoid, Trichogramma pretiosum Riley, collected from Riverside, CA (USA) produced a female-biased sex ratio of 0.24 (proportion of males). Six generations of sibling mating in the laboratory uncovered considerable inbreeding depression (∼ 20%) in fecundity and sex ratio. A population genetic study (based upon allozymes) showed the population was inbred (F it = 0.246), which corresponds to 56.6% sib-mating. However, average relatedness among females emerging from the same host egg was only 0.646, which is less than expected (0.75) if ovipositing females mate randomly. This lower relatedness could arise from inbreeding avoidance, multiple mating by females, or superparasitism. A review of the literature in general shows relatively low inbreeding depression in haplodiploid species, but indicates that inbreeding depression can be as high as that found in Drosophila. Finally, mating systems and inbreeding depression are thought to evolve in concert (in plants), but similar dynamic models of the joint evolution of sex ratio, mating systems, and inbreeding depression have not been developed for parasitoid wasps.

Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation

Understanding how and why populations evolve is of fundamental importance to molecular ecology. Restriction site‐associated DNA sequencing (RADseq), a popular reduced representation method, has ushered in a new era of genome‐scale research for assessing population structure, hybridization, demographic history, phylogeography and migration. RADseq has also been widely used to conduct genome scans to detect loci involved in adaptive divergence among natural populations. Here, we examine the capacity of those RADseq‐based genome scan studies to detect loci involved in local adaptation. To understand what proportion of the genome is missed by RADseq studies, we developed a simple model using different numbers of RAD‐tags, genome sizes and extents of linkage disequilibrium (length of haplotype blocks). Under the best‐case modelling scenario, we found that RADseq using six‐ or eight‐base pair cutting restriction enzymes would fail to sample many regions of the genome, especially for species with short linkage disequilibrium. We then surveyed recent studies that have used RADseq for genome scans and found that the median density of markers across these studies was 4.08 RAD‐tag markers per megabase (one marker per 245 kb). The length of linkage disequilibrium for many species is one to three orders of magnitude less than density of the typical recent RADseq study. Thus, we conclude that genome scans based on RADseq data alone, while useful for studies of neutral genetic variation and genetic population structure, will likely miss many loci under selection in studies of local adaptation.

GENETIC STRUCTURE OF A METAPOPULATION OF BLACK-TAILED PRAIRIE DOGS

Abstract Habitat alteration, agricultural control, recreational shooting, and most recently, sylvatic plague (caused by Yersinia pestis) contributed to local extinctions and a steady decline of black-tailed prairie dog (Cynomys ludovicianus) throughout its range. As a consequence, prairie dogs currently live in metapopulations, where their overall persistence will depend on a balance between extinction of colonies and recolonization from extant colonies. Patterns of genetic similarity among colonies, as measured by neutral molecular markers, provide an estimate of the dispersal and gene flow among colonies within prairie dog metapopulations. We sampled 13 colonies of black-tailed prairie dogs in short-grass prairie of northern Colorado, 100-km east of Fort Collins, Colorado. We used historical records and genetic analysis to show that colonies undergo regular extinctions, which subsequently are recolonized by individuals from multiple source colonies. We examined 155 individuals for variation at 7 microsatellite loci and found moderate levels of genetic differentiation among colonies (Θ [=FST] = 0.118). We also used assignment and exclusion tests based on multilocus genotypes of individuals to determine the probability that individuals originated from the same colony in which they were captured. About 39% of individuals could not be assigned to colonies where they were captured, indicating they were either immigrants (adults) or the offspring of immigrants (adults and juveniles). We tested for genetic isolation by distance among colonies by comparing genetic distances to geographic distances between colonies. Akaikes Information Criterion for model selection revealed that dispersal most likely occurred along low-lying dry creek drainages connecting isolated colonies. Genetic distances between colonies were also related to ages of colonies; older colonies were more similar genetically than younger colonies. This underscores the importance of dispersal among prairie dog colonies and has important implications for persistence of prairie dog metapopulations, in which all colonies, regardless of size, are vulnerable to extinction from plague.

Evolutionary relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA gene sequences.

Phylogenetic relationships among the Braconidae were examined using homologous 16S rDNA gene sequence data. Analyses recovered the few well‐supported relationships evident in this family from morphological analyses, viz the monophyly of the microgastroid complex of subfamilies, the monophyly of the cyclostome complex of subfamilies (=braconoids), a sister‐group relationship between the Alysiinae and Opiinae, and a close relationship between the Helconinae and Blacinae. With respect to the braconoid complex of subfamilies, a sister‐group relationship was recovered between Aphidiinae and Mesostoinae, and a clade composed of Gnamptodontinae + Histeromerinae + Rhyssalinae + Aphidiinae +Mesostoinae was also recovered. The Doryctinae and Rogadinae sensu lato (s.l.) were generally not resolved as monophyletic. With respect to the helconoid complex of subfamilies, a sister‐group relationship was recovered between Sigalphinae and Agathidinae, whereas Neoneurinae fell out among other helconoid subfamilies. Other relationships among the helconoid subfamilies were unclear from these analyses. With respect to the microgastroid complex of subfamilies, our data conform to morphological estimates, recovering ((Microgastrinae+Miracinae)+Cardiochilinae)+Cheloninae. The topology of our trees suggests that the cyclostome subfamilies are a natural derived group, inferring that endoparasitism (not ectoparasitism) is the ancestral state for the Braconidae, unless all of the ectoparasitic ancestors of the helconoid+microgastroid subfamilies are now extinct.

Molecular taxonomy using single‐strand conformation polymorphism (SSCP) analysis of mitochondrial ribosomal DNA genes

Single‐strand conformation polymorphism (SSCP) analysis detects single point mutations in DNA molecules. We demonstrate that SSCP analysis of mitochondrial ribosomal DNA (rDNA) genes is a sensitive taxonomic tool because these genes often differ at numerous sites among closely related species. Using conserved primers, portions of the 12S or 16S rDNA genes were amplified using the polymerase chain reaction (PCR) in congeneric species of ticks, leaf hoppers, mosquitoes, and closely related endoparasitic wasps. SSCP was performed and products were visualized with silver staining. Species‐specific patterns were observed in all taxa. Intraspecific variation at the level of single nucleotide substitutions was detected. SSCP diagnostics are less expensive and time consuming to develop than PCR with species‐specific primers, and, unlike PCR with arbitrary primers, there is minimal concern with DNA contamination from non‐target organisms.

THE POPULATION GENETICS OF SOMATIC MUTATION IN PLANTS

We hypothesize that somatic mutations may be the cause of variability among branches within individual trees, and that this variation is sufficient to deter herbivores. We discuss two single-locus genetic models of somatic mutation and consider how the organization of meristems affects somatic mutation rates. The models reveal that somatic mutation may be an important source of variation not only within trees but also within tree populations. If mutated buds have a selective advantage, the process may be even more important. Conditions under which somatic mutations may deter herbivores are restrictive, however, and finding variation at a single locus on an individual tree is highly improbable.