Andrew J. Bohonak

DISPERSAL, GENE FLOW, AND POPULATION STRUCTURE

The accuracy of gene flow estimates is unknown in most natural populations because direct estimates of dispersal are often not possible. These estimates can be highly imprecise or even biased because population genetic structure reflects more than a simple balance between genetic drift and gene flow. Most of the models used to estimate gene flow also assume very simple patterns of movement. As a result, multiple interpretations of population structure involving contemporary gene flow, departures from equilibrium, and other factors are almost always possible. One way to isolate the relative contribution of gene flow to population genetic differentiation is to utilize comparative methods. Population genetic statistics such as FST, heterozygosity and Neis D can be compared between species with differing dispersal abilities if these species are otherwise phylogenetically, geographically and demographically comparable. Accordingly, the available literature was searched for all groups that meet these criteria to determine whether broad conclusions regarding the relationships between dispersal, population genetic structure, and gene flow estimates are possible. Allozyme and mtDNA data were summarized for 27 animal groups in which dispersal differences can be characterized. In total, genetic data were obtained for 333 species of vertebrates and invertebrates from terrestrial, freshwater and marine habitats. Across these groups, dispersal ability was consistently related to population structure, with a mean rank correlation of -0.72 between ranked dispersal ability and FST. Gene flow estimates derived from private alleles were also correlated with dispersal ability, but were less widely available. Direct-count heterozygosity and average values of Neis D showed moderate degrees of correlation with dispersal ability. Thus, despite regional, taxonomic and methodological differences among the groups of species surveyed, available data demonstrate that dispersal makes a measurable contribution to population genetic differentiation in the majority of animal species in nature, and that gene flow estimates are rarely so overwhelmed by population history, departures from equilibrium, or other microevolutionary forces as to be uninformative.

Understanding the genetic effects of recent habitat fragmentation in the context of evolutionary history: Phylogeography and landscape genetics of a southern California endemic Jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus)

Habitat loss and fragmentation due to urbanization are the most pervasive threats to biodiversity in southern California. Loss of habitat and fragmentation can lower migration rates and genetic connectivity among remaining populations of native species, reducing genetic variability and increasing extinction risk. However, it may be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric fragmentation due to previous natural geological and climatic changes. To address these challenges, we examined the phylogenetic and population genetic structure of a flightless insect endemic to cismontane southern California, Stenopelmatus‘mahogani’ (Orthoptera: Stenopelmatidae). Analyses of mitochondrial DNA sequence data suggest that diversification across southern California began during the Pleistocene, with most haplotypes currently restricted to a single population. Patterns of genetic divergence correlate with contemporary urbanization, even after correcting for (geographical information system) GIS‐based reconstructions of fragmentation during the Pleistocene. Theoretical simulations confirm that contemporary patterns of genetic structure could be produced by recent urban fragmentation using biologically reasonable assumptions about model parameters. Diversity within populations was positively correlated with current fragment size, but not prehistoric fragment size, suggesting that the effects of increased drift following anthropogenic fragmentation are already being seen. Loss of genetic connectivity and diversity can hinder a populations ability to adapt to ecological perturbations commonly associated with urbanization, such as habitat degradation, climatic changes and introduced species. Consequently, our results underscore the importance of preserving and restoring landscape connectivity for long‐term persistence of low vagility native species.

Population structure of the pumpkin fruit fly Bactrocera depressa (Tephritidae) in Korea and Japan: Pliocene allopatry or recent invasion?

Because of their widespread agricultural impact and rapid range expansions, true fruit flies (Tephritidae) are the subject of quarantine and control efforts worldwide. Among these flies, the pumpkin fruit fly Bactrocera depressa, which infests squash and other cucurbitaceous plants in Korea, Japan and Taiwan, was recently isolated from produce shipments entering Japan and identified as a regulatory target. This species was described in 1933 from collections in Japan and discovered in 1974 in Korea, suggesting that it may have recently invaded mainland Asia. We analysed the genetic structure of Asian populations of B. depressa using sequence variation for mitochondrial gene cytochrome‐oxidase I and three nuclear loci: elongation factor 1α, tubulinβ1 and tubulinβ3, using frequency‐based approaches, nested clade analysis and assignment tests. Contrary to the hypothesis of recent invasion, high levels of genetic subdivision were found among five Korean and three Japanese populations. Nested clade analysis suggested a variety of processes operating over different time scales, including ancient isolation between Korea and Japan and more recent range expansions within each country. Contrary to a priori expectations, the results also suggested the recent introduction of a mitochondrial haplotype into Yokohama, Japan that is related closely to a widespread haplotype found throughout Korea. Assignment tests also supported these conclusions. The combination of a genealogical approach and probabilistic assignments of individuals to populations of origin was able to provide statistical support for the identification of cryptic introductions within an otherwise widespread indigenous species.

Copepod reproductive strategies : life-history theory, phylogenetic pattern and invasion of inland waters

Life-history theory predicts that different reproductive strategies should evolve in environments that differ in resource availability, mortality, seasonality, and in spatial or temporal variation. Within a population, the predicted optimal strategy is driven by tradeoffs that are mediated by the environment in which the organisms live. At the same time, phylogenetic history may circumscribe natural selection by dictating the range of phenotypes upon which selection can act, or by limiting the range of environments encountered. Comparisons of life-history patterns in related organisms provide a powerful tool for understanding both the nature of selection on life-history characters and the diversity of life-history patterns observed in nature. Here, we explore reproductive strategies of the Copepoda, a well defined group with many phylogenetically independent transitions from free-living to parasitic life styles, from marine to inland waters, and from active development to diapause. Most species are iteroparous annuals, and most (with the exception of some parasitic taxa) develop through a relatively restricted range of life-history stages (nauplii and copepodids, or some modification thereof). Within these bounds, we suggest that there may be a causal relationship between the success of numerous copepod taxa in inland waters and the prevalence of either diapause or parasitism within these groups. We hypothesize that inland waters are more variable spatially and temporally than marine habitats, and accordingly, we interpret diapause and parasitism as mechanisms for coping with environmental variance.

Invasion genetics of New World medflies: testing alternative colonization scenarios

The Mediterranean fruit fly (Ceratitis capitata) is an invasive agricultural pest with a wide host range and a nearly global distribution. Efforts to forgo the medflys spread into the United States are dependent on an understanding of population dynamics in newly established populations elsewhere. To explore the potential influence of demographic and historical parameters in six medfly populations distributed from Mexico to Peru, we created population genetic null models using Monte Carlo simulations. Null expectations for genetic differentiation (FST) were compared with actual sequence variation from four highly polymorphic nuclear loci. Four colonization scenarios that were modeled led to unique genetic signatures that could be used to interpret empirical data. Unless current gene flow across Latin America was assumed to be very high, we could reject colonizations consisting of multiple introductions, each of low genetic diversity. Further, if simulated populations were small (Ne = 5 × 102 individuals per population), small invasions from a single source consistently produced FST values comparable to those currently observed in Latin America. In contrast, only large invasions from diverse sources were compatible with the observed data for large populations (Ne ≥ 5 × 103). This study demonstrates that alternative population genetic hypotheses can be tested empirically even when departures from equilibrium are extreme, and that population genetic theory can be used to explore the processes that underlie biological invasions.

DISPERSAL OF INVERTEBRATES AMONG TEMPORARY PONDS: ARE GENETIC ESTIMATES ACCURATE?

Dispersal is difficult to quantify in most temporary pond invertebrates. As a consequence, researchers often infer the movement of individuals from indirect estimates of gene flow. Here, we review the assumptions associated with the most common gene flow estimate, which approximates migration using a simple island model and assumes equilibrium. Particular attention is focused on empirical studies of temporary pond invertebrates, where nonequilibrium conditions may be particularly important. When populations have not reached a long-term equilibrium between the migration of genes and random drift, estimates of movement can be biased dramatically. Eight comparative and theoretical tests for ascertaining these biases are described here. In some cases, specific hypotheses regarding contemporary and historical processes can also be tested statistically using computer simulations. Although the accuracy of gene flow estimates in temporary pond species varies widely, empirical and theoretical methods for assessing...

Loss of genetic connectivity and diversity in urban microreserves in a southern California endemic Jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus n. sp. ''santa monica'')

Microreserves may be useful in protecting native arthropod diversity in urbanized landscapes. However, species that do not disperse through the urban matrix may eventually be lost from these fragments. Population extinctions may be precipitated by an increase in genetic differentiation among fragments and loss of genetic diversity within fragments, and these effects should become stronger with time. We analyzed population genetic structure in the dispersal limited Jerusalem cricket Stenopelmatus n. sp. “santa monica” in the Santa Monica Mountains and Simi Hills north of Los Angeles, California (CA), to determine the impacts of fragmentation over the past 70 years. MtDNA divergence was greater among urban fragments than within contiguous habitat and was positively correlated with fragment age. MtDNA genetic diversity within fragments increased with fragment size and decreased with fragment age. Genetic divergence across 38 anonymous nuclear Inter-Simple Sequence Repeat (ISSR) loci was influenced by the presence of major highways and highway age, but there was no effect of additional urban fragmentation. ISSR diversity was not correlated with fragment size or age. Differing results between markers may be due to male-biased dispersal, or different effective population sizes, sorting rates, or mutation rates among sampled genes. Results suggest that genetic connectivity among populations has been disrupted by highways and urban development, prior to declines in local population sizes. We emphasize that genetic connectivity can rapidly erode in fragmented landscapes and that flightless arthropods can serve as sensitive indicators for these effects.

Genetic Signature of Rapid IHHNV (Infectious Hypodermal and Hematopoietic Necrosis Virus) Expansion in Wild Penaeus Shrimp Populations

Infectious hypodermal and hematopoietic necrosis virus (IHHNV) is a widely distributed single-stranded DNA parvovirus that has been responsible for major losses in wild and farmed penaeid shrimp populations on the northwestern Pacific coast of Mexico since the early 1990s. IHHNV has been considered a slow-evolving, stable virus because shrimp populations in this region have recovered to pre-epizootic levels, and limited nucleotide variation has been found in a small number of IHHNV isolates studied from this region. To gain insight into IHHNV evolutionary and population dynamics, we analyzed IHHNV capsid protein gene sequences from 89 Penaeus shrimp, along with 14 previously published sequences. Using Bayesian coalescent approaches, we calculated a mean rate of nucleotide substitution for IHHNV that was unexpectedly high (1.39×10−4 substitutions/site/year) and comparable to that reported for RNA viruses. We found more genetic diversity than previously reported for IHHNV isolates and highly significant subdivision among the viral populations in Mexican waters. Past changes in effective number of infections that we infer from Bayesian skyline plots closely correspond to IHHNV epizootiological historical records. Given the high evolutionary rate and the observed regional isolation of IHHNV in shrimp populations in the Gulf of California, we suggest regular monitoring of wild and farmed shrimp and restriction of shrimp movement as preventative measures for future viral outbreaks.

Is population genetics mired in the past

In a recent TREE perspective, Bossart and Prowell1 concluded that researchers estimating population structure used antiquated methods, and failed to acknowledge and test underlying model assumptions. We found these conclusions surprisingly pessimistic and decided to examine 67 papers on population structure from Evolution and Molecular Ecology (1997). Although many studies in Evolution were based solely on allozymes (12/25), this was true of only 1/28 papers in Molecular Ecology. The journal bias might explain some of Bossart and Prowell’s findings, because they reviewed papers in Evolution that tended to focus primarily on theoretical problems in evolution, and only secondarily on estimating population structure. We found neither that ‘cautions [regarding analyses of population structure] have not been widely embraced by the scientific community’, nor that ‘conclusions often are drawn ... even though there are multiple, equally viable interpretations’1. Only 14/67 papers calculated Nm (gene flow) and only two interpreted Nm literally. Most researchers viewed their results from a number of perspectives (e.g. historical association versus contemporary gene flow), and it was nearly impossible to find studies that did not use multiple loci and conduct sensitivity analyses over loci and/or populations. Departures from equilibrium undoubtedly bias gene flow estimates in many cases. However, we disagree that allozymes yield no useful information regarding the movement of individuals. How can we test this assertion? Bossart and Prowell stated that comparisons with direct estimates of dispersal are ‘the only valid approach to the study and interpretation of gene flow in an ecological context’. We had difficulty interpreting this statement because it is well known that dispersal and gene flow are not equivalent for many reasons, and that rare dispersal events overlooked in most ecological studies can heavily influence indirect gene flow estimates2,3. Furthermore, there are other valid approaches for appraising gene flow estimates, such as examining correlations between Fst and morphological indicators of dispersal ability. It has been repeatedly shown that larval time is correlated with population differentiation in marine invertebrates4,5 and vertebrates6, flightless insects tend to have higher values of Fst than flightform insects7–11, and Fst values in plants are related to mode of seed dispersal12. These are not isolated examples; three separate reviews have found that wide dispersers tend to have higher estimates of Nm and lower estimates of Fst than those with restricted dispersal13–15. If ongoing gene flow has a negligible impact on allozyme differentiation among populations, there should be no correlation between population genetic differentiation and any measure of dispersal ability. To conclude that population genetics is ‘no longer advancing [because of] our reliance on easy to apply, conventional indirect methods’ implies that: (1) most evolutionary biologists use allozymes and F-statistics, and (2) this has stagnated the field. Yet the exclusive use of allozymes is becoming rarer and new statistical methodologies are published almost monthly. Therefore, we take a less pessimistic view than Bossart and Prowell. We believe that the limitations of traditional approaches are generally understood and that they still provide a valuable first approximation in many cases. Methods for determining the relative contributions of history and current gene flow are already being developed and utilized. Judging from the recent literature, we would argue that advancement, not stagnation, is the current state of the field.

The value of DNA sequence data for studying landscape genetics.

In a recent Opinion article in Molecular Ecology, Wang (2010) emphasizes the fact that current patterns of genetic differentiation among populations reflect processes that have acted over temporal scales ranging from contemporary to ancient. He draws a sharp distinction between the fields of phylogeography (as the study of historical processes) and landscape genetics (which he restricts to very recent processes). Wang characterizes DNA sequence data as being inappropriate for the study of contemporary population processes and further states that studies which only include mitochondrial DNA or chloroplast DNA data cannot be considered part of landscape genetics. In this response, we clarify the generally accepted view that DNA sequence data can be analysed with methods that separate contemporary and historical processes. To illustrate this point, we summarize the study of Vandergast et al. (2007), which Wang mischaracterizes as being confused in terms of temporal scale. Although additional focus should be placed on the important issue of correct data interpretation, we disagree strongly with the implication that contemporary and historic processes cannot be separated in the analyses of DNA sequence data.