Surviving background extinction: Inferences from historic and current dynamics in the contrasting population structures of two endemic Mexican cycads

Ecological and microevolutionary perspectives were used to investigate signs of background extinction in two endemic species. We studied relict populations of the cycad Dioon caputoi, contrasting its population structure and neighborhood size with those of Dioon planifolium as a demographically healthier reference population. Population dynamics analysis was performed on two populations of D. caputoi through Integral Projection Models and genetic neighborhoods compared between species through 172 Inter Simple Sequence Repeat loci performed in one population of each of the two study species. The D. caputoi populations mostly comprised adult plants, while D. planifolium presented mainly juvenile individuals. Dioon caputoi showed equilibrium in population growth (i.e., λ ≈ 1), with low recruitment, and its genetic neighborhood revealed highly related individuals in a unique distance class (r_ij = 0.407, 33 m). A contrasting pattern was found in D. planifolium, which showed higher relatedness in the first distance class (r_ij = 0.543, 5 m), gradually decreasing to 20 m. The discrepancies between the two species reflect different strategies of persistence. Dioon caputoi conserves a relict dynamics with signs of a multigenerational, attritional loss of reproductive fitness, while D. planifolium does not. This study furthers our understanding of the background extinction process and the information will thus contribute to the management and conservation of this endangered species.     

An integrated population model sheds light on the complex population dynamics of a unique colonial breeder

Climate models forecast increasing climatic variation and more extreme events, which could increase the variability in animal demographic rates. More variable demographic rates generally lead to lower population growth and can be detrimental to wild populations, especially if the particular demographic rates affected are those to which population growth is most sensitive. We investigated the population dynamics of a metapopulation of 25 colonies of a semi-arid bird species, the sociable weaver Philetairus socius, and how it was influenced by seasonal weather during 1993–2014. We constructed an integrated population model which estimated population sizes similar to observed population counts, and allowed us to estimate annual fecundity and recruitment. Variance in fecundity contributed most to variance in population growth, which showed no trend over time. No weather variables explained overall demographic variation at the population level. However, a separate analysis of the largest colony showed a clear decline with a high extinction probability (0.05 to 0.33) within 5 years after the study period. In this colony, juvenile survival was lower when summers were hot, and adult survival was lower when winters were cold. Rainfall was also negatively correlated with adult survival. These weather effects could be due to increased physiological demands of thermoregulation and rainfall-induced breeding activity. Our results suggest that the dynamics of the population on the whole are buffered against current weather variation, as individual colonies apparently react in different ways. However, if more and increasingly extreme weather events synchronize colony dynamics, they are likely to have negative effects.     

Estimability of migration survival rates from integrated breeding and winter capture–recapture data

Long‐distance migration is a common phenomenon across the animal kingdom but the scale of annual migratory movements has made it difficult for researchers to estimate survival rates during these periods of the annual cycle. Estimating migration survival is particularly challenging for small‐bodied species that cannot carry satellite tags, a group that includes the vast majority of migratory species. When capture–recapture data are available for linked breeding and non‐breeding populations, estimation of overall migration survival is possible but current methods do not allow separate estimation of spring and autumn survival rates. Recent development of a Bayesian integrated survival model has provided a method to separately estimate the latent spring and autumn survival rates using capture–recapture data, though the accuracy and precision of these estimates has not been formally tested. Here, I used simulated data to explore the estimability of migration survival rates using this model. Under a variety of biologically realistic scenarios, I demonstrate that spring and autumn migration survival can be estimated from the integrated survival model, though estimates are biased toward the overall migration survival probability. The direction and magnitude of this bias are influenced by the relative difference in spring and autumn survival rates as well as the degree of annual variation in these rates. The inclusion of covariates can improve the model's performance, especially when annual variation in migration survival rates is low. Migration survival rates can be estimated from relatively short time series (4–5 years), but bias and precision of estimates are improved when longer time series (10–12 years) are available. The ability to estimate seasonal survival rates of small, migratory organisms opens the door to advancing our understanding of the ecology and conservation of these species. Application of this method will enable researchers to better understand when mortality occurs across the annual cycle and how the migratory periods contribute to population dynamics. Integrating summer and winter capture data requires knowledge of the migratory connectivity of sampled populations and therefore efforts to simultaneously collect both survival and tracking data should be a high priority, especially for species of conservation concern.     

Pitfalls to avoid in nonlinear perturbation analysis of structured population models

Despite the ubiquity of nonlinear functional relationships in nature we tend to characterize mechanisms in science using more tractable linear functions. In demographic modeling, transfer function analysis is used to calculate the nonlinear response of population growth rate to a theoretical perturbation of one or more matrix elements. This elegant approach is not yet popular in ecology. Inconveniently, using transfer function without care can produce erroneous results without warning. We used a large matrix projection model database to explore the potential pitfalls to be avoided in using transfer function analysis. We asked a fundamental population control question, what matrix element perturbation would be needed to reach a minimum goal of replacement population growth? We then tracked instances in which transfer function yields erroneous output and explored these cases in detail to measure how frequently it occurs. We developed a phylogenetically-corrected mixed effects logistic regression model in a Bayesian framework to test the effect of species traits and the identity of matrix elements on the probability that transfer function yields errors. We found in 16% of cases the transfer function yielded erroneous outcomes. These errors were more likely when perturbing demographic stasis and also for shrubs more than any other life form. Errors in transfer function analysis were often due to perturbing matrix elements beyond their biological limits, even when this is still mathematically correct. To use transfer function analysis properly in demographic modeling and avoid erroneous results, input must be carefully selected to include only a biologically admissible set of perturbations.     

Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demography

Abstract The respective role of factors acting on population functioning can be inferred from a variety of approaches, including population genetics and demography. We here investigated the role of four of these factors (mating systems, population size, bottlenecks and migration) in the hermaphroditic freshwater snail Physa acuta. Twenty-four populations were sampled either around Montpellier (local scale), or at the scale of France (global scale). At local scale, eight populations were sampled twice, before and after summer drying out. The genetic structure of these populations was studied using microsatellite loci. Populations were classified according to openness (ponds vs. rivers) and water regime (permanent vs. temporary) allowing predictions on genetic patterns (e.g. diversity within populations and differentiation). At local scale, progeny-arrays analysis of the selfing rate was conducted, and size distributions of individuals were followed over two years. Results with regard to the four factors mentioned above were: (i) Estimates of population selfing rates derived from inbreeding coefficients were only slightly higher than those from progeny-arrays. (ii) More variation was detected in rivers than in ponds, but no influence of water regime was detected. One reason might be that permanent populations are not going less often through low densities than those from temporary habitats at the time scale studied. (iii) There was limited evidence for genetic bottlenecks which is compatible with the fact that even marked reduction in water availability was not necessarily associated with demographic bottlenecks. More generally, bottlenecks reducing genetic variation probably occur at population foundation. (iv) Lower genetic differentiation was detected among rivers than among ponds which might be related to limitations on gene flow. Demographic and temporal genetic data further indicates that flooding in rivers is unlikely to induce marked gene flow explaining the strong genetic differentiation at short geographical scale in such habitats. Finally, the demographic data suggest that some populations are transitory and subject to recurrent recolonization, a pattern that was also detected through genetic data.     

Genetic structure of desert ground squirrels over a 20-degree-latitude transect from Oregon through the Baja California peninsula

The genetic structure of populations over a wide geographical area should reflect the demographic and evolutionary processes that have shaped a species across its range. We examined the population genetic structure of antelope ground squirrels (Ammospermophilus leucurus) across the complex of North American deserts from the Great Basin of Oregon to the cape region of the Baja California peninsula. We sampled 73 individuals from 13 major localities over this 2500-km transect, from 43 to 22 degrees north. Our molecular phylogeographical analysis of 555 bp of the mitochondrial cytochrome b gene and 510 bp of the control region revealed great genetic uniformity in a single clade that extends from Oregon to central Baja California. A second distinct clade occupies the southern half of the peninsula. The minimal geographical structure of the northern clade, its low haplotype diversity and the distribution of pairwise differences between haplotypes suggest a rapid northward expansion of the population that must have followed a northward desert habitat shift associated with the most recent Quaternary climate warming and glacial retreat. The higher haplotype diversity within the southern clade and distribution of pairwise differences between haplotypes suggest that the southern clade has a longer, more stable history associated with a southern peninsular refugium. This system, as observed, reflects both historical and contemporary ecological and evolutionary responses to physical environmental gradients within genetically homogeneous populations.     

The burgeoning field of statistical phylogeography

In the newly emerging field of statistical phylogeography, consideration of the stochastic nature of genetic processes and explicit reference to theoretical expectations under various models has dramatically transformed how historical processes are studied. Rather than being restricted to ad hoc explanations for observed patterns of genetic variation, assessments about the underlying evolutionary processes are now based on statistical tests of various hypotheses, as well as estimates of the parameters specified by the models. A wide range of demographical and biogeographical processes can be accommodated by these new analytical approaches, providing biologically more realistic models. Because of these advances, statistical phylogeography can provide unprecedented insights about a species' history, including decisive information about the factors that shape patterns of genetic variation, species distributions, and speciation. However, to improve our understanding of such processes, a critical examination and appreciation of the inherent difficulties of historical inference and challenges specific to testing phylogeographical hypotheses are essential. As the field of statistical phylogeography continues to take shape many difficulties have been resolved. Nonetheless, careful attention to the complexities of testing historical hypotheses and further theoretical developments are essential to improving the accuracy of our conclusions about a species' history.     

Growth and architecture of small honey mesquites under jackrabbit browsing: overcoming the disadvantage of being eaten

Browsing is an important mortality factor in seedlings and small plants. However, the induced changes in the architecture of plant survivors may influence subsequent browsing, opening the possibility of compensating for the damage done. How jackrabbit (Lepus californicus) browsing affects the growth and architecture of small individuals of honey mesquite, Prosopis glandulosa var. torreyana, a tree/shrub that produces spines at every node, was explored. Naturally established mesquites of unknown age were selected in one site, and 2-year-old mesquites were transplanted in another site. In both cases, half of them were exposed to jackrabbits and the other half were excluded as controls. After 4 years, shoot production (height, length and number of derived shoots) and plant growth (height and cover) increased 1.4-2.5-fold in naturally established controls relative to exposed plants, depending on the measured variable. In the transplant experiment, the increases were 2.8-7.1-fold in controls relative to exposed plants 2 years after initiation of the experiment. The net loss of biomass in treatment vs. control plants in these experiments suggests a negative response to browsing which has been defined as under-compensation. Alternative architectures in honey mesquites were evident at the end of the exclusion experiments: controls had long branches and an extended crown cover, while exposed plants had short branches and a compact crown cover. Results indicated that mesquites were able to grow under browser pressure by packing many stems in a compact matrix armed with spines and producing one or more shoots tall and wide enough to escape from jackrabbits.     

Sexual differences in reproductive phenology and their consequences for the demography of Baccharis dracunculifolia (Asteraceae), a dioecious tropical shrub

Patterns of phenological variation and reproductive investment were studied in the dioecious shrub Baccharis dracunculifolia DC (Asteraceae), and possible consequences on survivorship were evaluated. The sex ratio was determined in a natural field population (n = 921) of B. dracunculifolia in Belo Horizonte, Brazil. Fifty-two males and 56 females were sampled at random from this population. During the reproductive season of 1999, inflorescence production, shoot growth and mortality, and xylem water potential were recorded for each individual. The population sex ratio was male-biased (1.27 : 1, P < 0.05), and was associated with a higher mortality of female shoots (38.4 vs. 23.1 %, P < 0.05), and individuals (17.8 vs. 11.5 %, P < 0.1), despite lower water stress in female plants. Flowering phenology also differed between the sexes, with males producing more inflorescences, and earlier, than females. Owing to fruit maturation, the number of inflorescences supported by females was higher than that supported by males later in the reproductive season. This occurred during the dry season, and drought stress may have been responsible for the greater female mortality. Thus, the male-biased sex ratio in this population of B. dracunculifolia is probably due to different reproductive functions of males and females. Intersexual differences in reproductive phenology had consequences for plant demography.