An ecological approach to measuring the evolutionary consequences of gene flow from crops to wild or weedy relatives.

PREMISE OF THE STUDY: Agricultural practices routinely create opportunities for crops to hybridize with wild relatives, leading to crop gene introgression into wild genomes. Conservationists typically worry this introgression could lead to genetic homogenization of wild populations, over and above the central concern of transgene escape. Alternatively, viewing introgression as analogous to species invasion, we suggest that increased genetic diversity may likewise be an undesirable outcome. METHODS: Here, we compare the sensitivity of conventional population genetic metrics with species diversity indices as indicators of the impact of gene flow on genetic diversity. We illustrate this novel approach using multilocus genotype data (12 allozyme loci) from 10 wild (Beta vulgaris subsp. maritima) and eight putative crop-wild hybrid beet populations (B. vulgaris subsp. vulgaris × B. vulgaris subsp. maritima) scattered throughout Europe. RESULTS: Conventional population genetic metrics mostly failed to detect shifts in genetic composition of putative hybrid populations. By contrast, species diversity indices unambiguously revealed increased genetic diversity in putative hybrid populations. DISCUSSION: We encourage other workers to explore the utility of our more sensitive approach for risk assessment prior to the release of transgenic crops, with a view toward widespread adoption of our method in studies aimed at detecting allelic invasion.

Efficacy of land-cover models in predicting isolation of marbled salamander populations in a fragmented landscape.

Amphibians worldwide are facing rapid declines due to habitat loss and fragmentation, disease, and other causes. Where habitat alteration is implicated, there is a need for spatially explicit conservation plans. Models built with geographic information systems (GIS) are frequently used to inform such planning. We explored the potential for using GIS models of functional landscape connectivity as a reliable proxy for genetically derived measures of population isolation. We used genetic assignment tests to characterize isolation of marbled salamander populations and evaluated whether the relative amount of modified habitat around breeding ponds was a reliable indicator of population isolation. Using a resampling analysis, we determined whether certain land-cover variables consistently described population isolation. We randomly drew half the data for model building and tested the performance of the best models on the other half 100 times. Deciduous forest was consistently associated with lower levels of population isolation, whereas salamander populations in regions of agriculture and anthropogenic development were more isolated. Models that included these variables and pond size explained 65-70% of variation in genetically inferred isolation across sites. The resampling analysis confirmed that these habitat variables were consistently good predictors of isolation. Used judiciously, simple GIS models with key land-cover variables can be used to estimate population isolation if field sampling and genetic analysis are not possible.

Preference for oddity: uniqueness heuristic or hierarchical choice process?

Traditional economic theories assume decision makers in multialternative choice tasks "assign" a value to each option and then express rational preferences. Here, I report an apparent violation of such rationality in gray jays (Perisoreus canadensis). I tested the jays' preference in a quaternary choice task where three options were the same color and the fourth option was a different color. All options offered an identical food reward and so the strictly rational expectation was that subjects would choose the odd-colored option in 25% of choices. In clear disagreement, every subject chose the odd option more frequently than expected. I speculate as to how this surprising preference for oddity might have been ecologically rational: by using a unique-choice heuristic, the jays might have been able to bypass a deliberative phase of the decision process and devote more attention to scanning for predators. Alternatively, it is conceivable that the jays did not prefer oddity per se. Instead, they might have used a hierarchical process, assigning options to color categories and then choosing between categories. If so, their behavior matches expectation after all (on average, subjects chose the odd option 50% of the time). It should be straightforward to test these competing hypotheses. The current results can be viewed as a new example of how simple mechanisms sometimes produce economically puzzling yet ecologically rational decision making.

State-dependent choice and ecological rationality.

Decision makers who minimize costly errors should flexibly adjust the way they trade off competing demands, depending on their current state. We explore how state (amount of hoarded food) affects willingness to take extra predation risk to obtain larger food rewards, particularly in animals that may overemphasize safety. Assuming a sigmoid fitness function, we explore how a supplement in state influences this willingness trade danger for food energy. Above a threshold, the model predicts the supplement will weaken this willingness. Incremental increases in state in the deceleratory phase yield smaller fitness gains, so it pays to increase emphasis on safety after receiving a supplement. Below this threshold, the model makes the opposite prediction because incremental increases in state yield bigger fitness gains and so it pays to decrease emphasis on safety. We use the model to explain why hoarding gray jays (Perisoreus canadensis) were induced by an experimental subsidy to accept greater danger. This formerly puzzling finding makes sense if the jays' effective hoard was relatively small, due to theft and decomposition. We discuss adaptive state-dependent choice as a general explanation for apparently irrational behavior.

Climate change and the demographic demise of a hoarding bird living on the edge.

Population declines along the lower-latitude edge of a species' range may be diagnostic of climate change. We report evidence that climate change has contributed to deteriorating reproductive success in a rapidly declining population of the grey jay (Perisoreus canadensis) at the southern edge of its range. This non-migratory bird of boreal and subalpine forest lives on permanent territories, where it hoards enormous amounts of food for winter and then breeds very early, under still-wintry conditions. We hypothesized that warmer autumns have increased the perishability of hoards and compromised subsequent breeding attempts. Our analysis confirmed that warm autumns, especially when followed by cold late winters, have led to delayed breeding and reduced reproductive success. Our findings uniquely show that weather months before the breeding season impact the timing and success of breeding. Warm autumns apparently represent hostile conditions for this species, because it relies on cold storage. Our study population may be especially vulnerable, because it is situated at the southern edge of the range, where the potential for hoard rot is most pronounced. This population's demise may signal a climate-driven range contraction through local extinctions along the trailing edge.

Interruptions improve choice performance in gray jays: prolonged information processing versus minimization of costly errors.

Under the assumption that selection favors minimization of costly errors, erroneous choice may be common when its fitness cost is low. According to an adaptive-choice model, this cost depends on the rate at which an animal encounters the choice: the higher this rate, the smaller the cost of choosing a less valuable option. Errors should thus be more common when interruptions to foraging are shorter. A previous experiment supported this prediction: gray jays, Perisoreus canadensis, were more error prone when subjected to shorter delays to access to food rewards. This pattern, though, is also predicted by an attentional-constraints model. Because the subjects were able to inspect the rewards during delays, their improved performance when subjected to longer delays could have been a byproduct of the experimentally prolonged opportunity for information processing. To evaluate this possibility, a follow-up experiment manipulated both delay to access and whether rewards could be inspected during delays. Depriving jays of the opportunity to inspect rewards (using opaque lids) induced only a small, nonsignificant increase in error rate. This effect was independent of length of delay and so the jays' improved performance when subjected to longer delays was not simply a byproduct of prolonged information processing. More definitively, even when the jays were prevented from inspecting rewards during delays, their performance improved when subjected to longer delays. The findings are thus consistent with the adaptive-choice model.

Population Variability and Extinction Risk.

Population models generally predict increased extinction risk (ER) with increased population variability ( PV  ), yet some empirical tests have provided contradictory findings. We resolve this conflict by attributing negative measured relationships to a statistical artifact that arises because PV tends to be underestimated for populations with short persistence. Such populations do not go extinct quickly as a consequence of low intrinsic variability; instead, the measured variability is low because they go extinct so quickly. Consequently, any underlying positive relationship between PV and ER tends to be obscured. We conducted a series of analyses to evaluate this claim. Simulations showed that negative measured relationships are to be expected, despite an underlying positive relationship. Simulations also identified properties of data, minimizing this bias and thereby permitting meaningful analysis. Experimental data on laboratory populations of a bruchid beetle (Callosobruchus maculatus) supported the simulation results. Likewise, with an appropriate statistical approach (Cox regression on untransformed data), reanalysis of a controversial data set on British island bird populations revealed a significant positive association between PV and ER (p = 0.03). Finally, a similar analysis of time series for naturally regulated animal populations revealed a positive association between PV and quasiextinction risk (p < 0.01). Without exception, our simulation results, experimental findings, reanalysis of published data, and analysis of quasiextinction risk all contradict previous reports of negative or equivocal relationships. Valid analysis of meaningful data provides strong evidence that increased population variability leads to increased extinction risk.

RESUMEN: Los modelos poblacionales generalmente predicen un mayor riesgo de extinción (ER) al aumentar la variabilidad poblacional ( PV  ), a pesar de ello, algunas pruebas empíricas han proporcionado resultados contradictorios. Nosotros hemos resuelto este conflicto mediante la atribución de mediciones de relaciones negativas a un producto estadístico que surge debido a que la PV tiende a ser subestimada para poblaciones de persistencia corta. Estas poblaciones no se extinguen rápidamente como resultado de una variabilidad intrínseca baja; por lo contrario, la variabilidad medida es baja debido a que las poblaciones se extinguen tan rápidamente. Consecuentemente, cualquier relación positiva subyacente entre la PV y el ER tienden a ser opacadas. Llevamos a cabo una serie de análisis para evaluar este argumento. Las simulaciones mostraron que las relaciones negativas medidas son de esperarse, a pesar de una relación positiva subyacente. Las simulaciones también identificaron propiedades de los datos que minimizan este sesgo y por lo tanto permiten un análisis significativo. Los datos experimentales en poblaciones de laboratorio de un coleóptero bruchidae (Callosobruchus maculatus) respaldan los resultados de las simulaciones. De la misma manera, el uso de una técnica estadística adecuada (por ejemplo, la regresión Cox en datos sin transformar), usada en la repetición del análisis de un juego de datos controvertidos de poblaciones de aves de la Isla Británica reveló una asociación positiva significativa entre la PV y el ER (p = 0.03). Finalmente, un análisis similar de series de tiempo para poblaciones de animales reguladas de manera natural revelaron una asociación positiva entre la PV y el riesgo de cuasi-extinción (p < 0.01). Sin excepciones, nuestros resultados de simulaciones, los resultados experimentales, la repetición del análisis de datos publicados, y el análisis de riesgo de cuasi-extinción contradicen informes previos de relaciones negativas o equívocas. Los análisis válidos de datos significativos proveen una evidencia sólida de que los incrementos en la variabilidad poblacional conducen a un incremento en el riego de extinción.