Amy L. Russell

Moving across the border: modeling migratory bat populations

The migration of animals across long distances and between multiple habitats presents a major challenge for conservation. For the migratory Mexican free-tailed bat (Tadarida brasiliensis mexicana), these challenges include identifying and protecting migratory routes and critical roosts in two countries, the United States and Mexico. Knowledge and conservation of bat migratory routes is critical in the face of increasing threats from climate change and wind turbines that might decrease migratory survival. We employ a new modeling approach for bat migration, network modeling, to simulate migratory routes between winter habitat in southern Mexico and summer breeding habitat in northern Mexico and the southwestern United States. We use the model to identify key migratory routes and the roosts of greatest conservation value to the overall population. We measure roost importance by the degree to which the overall bat population declined when the roost was removed from the model. The major migratory routes—those with the greatest number of migrants—were between winter habitat in southern Mexico and summer breeding roosts in Texas and the northern Mexican states of Sonora and Nuevo Leon. The summer breeding roosts in Texas, Sonora, and Nuevo Leon were the most important for maintaining population numbers and network structure - these are also the largest roosts. This modeling approach contributes to conservation efforts by identifying the most influential areas for bat populations, and can be used to as a tool to improve our understanding of bat migration for other species. We anticipate this approach will help direct coordination of habitat protection across borders.

A new species of Emballonura (Chiroptera: Emballonuridae) from the dry regions of Madagascar

Abstract We describe a new species of bat in the genus Emballonura (Chiroptera: Emballonuridae), E. tiavato, from the dry forest regions of Madagascar. This species is distinguished from the only other member of this genus found on the island, E. atrata, and extralimital species based on a variety of external and cranial characteristics. Details of the distribution, phylogeny, and natural history of the two species of Malagasy Emballonura are presented.

Market forces and technological substitutes cause fluctuations in the value of bat pest-control services for cotton

Critics of the market-based, ecosystem services approach to biodiversity conservation worry that volatile market conditions and technological substitutes will diminish the value of ecosystem services and obviate the “economic benefits” arguments for conservation. To explore the effects of market forces and substitutes on service values, we assessed how the value of the pest-control services provided by Mexican free-tailed bats (Tadarida brasiliensis mexicana) to cotton production in the southwestern U.S. has changed over time. We calculated service values each year from 1990 through 2008 by estimating the value of avoided crop damage and the reduced social and private costs of insecticide use in the presence of bats. Over this period, the ecosystem service value declined by 79% (

Exploring Demographic, Physical, and Historical Explanations for the Genetic Structure of Two Lineages of Greater Antillean Bats

19.09 million U.S. dollars) due to the introduction and widespread adoption of Bt (Bacillus thuringiensis) cotton transgenically modified to express its own pesticide, falling global cotton prices and the reduction in the number of hectares in the U.S. planted with cotton. Our results demonstrate that fluctuations in market conditions can cause temporal variation in ecosystem service values even when ecosystem function – in this case bat population numbers – is held constant. Evidence is accumulating, however, of the evolution of pest resistance to Bt cotton, suggesting that the value of bat pest-control services may increase again. This gives rise to an economic option value argument for conserving Mexican free-tailed bat populations. We anticipate that these results will spur discussion about the role of ecosystem services in biodiversity conservation in general, and bat conservation in particular.

Population growth of Mexican free-tailed bats (Tadarida brasiliensis mexicana) predates human agricultural activity.

Observed patterns of genetic structure result from the interactions of demographic, physical, and historical influences on gene flow. The particular strength of various factors in governing gene flow, however, may differ between species in biologically relevant ways. We investigated the role of demographic factors (population size and sex-biased dispersal) and physical features (geographic distance, island size and climatological winds) on patterns of genetic structure and gene flow for two lineages of Greater Antillean bats. We used microsatellite genetic data to estimate demographic characteristics, infer population genetic structure, and estimate gene flow among island populations of Erophylla sezekorni/E. bombifrons and Macrotus waterhousii (Chiroptera: Phyllostomidae). Using a landscape genetics approach, we asked if geographic distance, island size, or climatological winds mediate historical gene flow in this system. Samples from 13 islands spanning Erophyllas range clustered into five genetically distinct populations. Samples of M. waterhousii from eight islands represented eight genetically distinct populations. While we found evidence that a majority of historical gene flow between genetic populations was asymmetric for both lineages, we were not able to entirely rule out incomplete lineage sorting in generating this pattern. We found no evidence of contemporary gene flow except between two genetic populations of Erophylla. Both lineages exhibited significant isolation by geographic distance. Patterns of genetic structure and gene flow, however, were not explained by differences in relative effective population sizes, island area, sex-biased dispersal (tested only for Erophylla), or surface-level climatological winds. Gene flow among islands appears to be highly restricted, particularly for M. waterhousii, and we suggest that this species deserves increased taxonomic attention and conservation concern.

Genetic Structure of Little Brown Bats (Myotis lucifugus) Corresponds with Spread of White-Nose Syndrome among Hibernacula

BackgroundHuman activities, such as agriculture, hunting, and habitat modification, exert a significant effect on native species. Although many species have suffered population declines, increased population fragmentation, or even extinction in connection with these human impacts, others seem to have benefitted from human modification of their habitat. Here we examine whether population growth in an insectivorous bat (Tadarida brasiliensis mexicana) can be attributed to the widespread expansion of agriculture in North America following European settlement. Colonies of T. b. mexicana are extremely large (~106 individuals) and, in the modern era, major agricultural insect pests form an important component of their food resource. It is thus hypothesized that the growth of these insectivorous bat populations was coupled to the expansion of agricultural land use in North America over the last few centuries.ResultsWe sequenced one haploid and one autosomal locus to determine the rate and time of onset of population growth in T. b. mexicana. Using an approximate Maximum Likelihood method, we have determined that T. b. mexicana populations began to grow ~220 kya from a relatively small ancestral effective population size before reaching the large effective population size observed today.ConclusionsOur analyses reject the hypothesis that T. b. mexicana populations grew in connection with the expansion of human agriculture in North America, and instead suggest that this growth commenced long before the arrival of humans. As T. brasiliensis is a subtropical species, we hypothesize that the observed signals of population growth may instead reflect range expansions of ancestral bat populations from southern glacial refugia during the tail end of the Pleistocene.

Deglaciation explains bat extinction in the Caribbean

Until recently, the little brown bat (Myotis lucifugus) was one of the most common bat species in North America. However, this species currently faces a significant threat from the emerging fungal disease white-nose syndrome (WNS). The aims of this study were to examine the population genetic structure of M. lucifugus hibernating colonies in Pennsylvania (PA) and West Virginia (WV), and to determine whether that population structure may have influenced the pattern of spread of WNS. Samples were obtained from 198 individuals from both uninfected and recently infected colonies located at the crest of the disease front. Both mitochondrial (636bp of cytochrome oxidase I) and nuclear (8 microsatellites) loci were examined. Although no substructure was evident from nuclear DNA, female-mediated gene flow was restricted between hibernacula in western PA and the remaining colonies in eastern and central PA and WV. This mitochondrial genetic structure mirrors topographic variation across the region: 3 hibernating colonies located on the western Appalachian plateau were significantly differentiated from colonies located in the central mountainous and eastern lowland regions, suggesting reduced gene flow between these clusters of colonies. Consistent with the hypothesis that WNS is transmitted primarily through bat-to-bat contact, these same 3 hibernating colonies in westernmost PA remained WNS-free for 1-2 years after the disease had swept through the rest of the state, suggesting that female migration patterns may influence the spread of WNS across the landscape.

Sex-biased dispersal produces high error rates in mitochondrial distance-based and tree-based species delimitation

Ecological factors such as changing climate on land and interspecific competition have been debated as possible causes of postglacial Caribbean extinction. These hypotheses, however, have not been tested against a null model of climate-driven postglacial area loss. Here, we use a new Quaternary mammal database and deep-sea bathymetry to estimate species–area relationships (SARs) at present and during the Last Glacial Maximum (LGM) for bats of the Caribbean, and to model species loss as a function of area loss from rising sea level. Island area was a significant predictor of species richness in the Bahamas, Greater Antilles, and Lesser Antilles at all time periods, except for the Lesser Antilles during the LGM. Parameters of LGM and current SARs were similar in the Bahamas and Greater Antilles, but not the Lesser Antilles, which had fewer estimated species during the LGM than expected given their size. Estimated postglacial species losses in the Bahamas and Greater Antilles were largely explained by inferred area loss from rising sea level in the Holocene. However, there were more species in the Bahamas at present, and fewer species in the smaller Greater Antilles, than expected given island size and the end-Pleistocene/early Holocene SARs. Poor fossil sampling and ecological factors may explain these departures from the null. Our analyses illustrate the importance of changes in area in explaining patterns of species richness through time and emphasize the role of the SAR as a null hypothesis in explorations of the impact of novel ecological interactions on extinction.

Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species

Abstract Species delimitation using mitochondrial sequences aims to identify species as morphological expertise and biodiversity both decline. Species delimitation in animals relies completely or in part on 2 criteria: genetic distance and reciprocal monophyly. Using coalescent simulations of populations experiencing continuous and interrupted gene flow we show that these commonly applied criteria incur both high false-positive and high false-negative error rates in species delimitation when dispersal is sex biased, as it is in most mammals. The combination of distance- and topology-based criteria will incur false-positive error rates well above 5% when ancestral effective population sizes are large and when population structure has been in place for 10,000 years or more. This effect persists even with a subtle bias in dispersal of 1 : 4 female : males dispersing in each generation. High false-positive error rates in genetic distances can be overcome by correcting for within-population sequence divergence. We argue that mitochondrial species delimitation requires additional supporting data on ecology, behavior, and morphology, as well as within-population sampling of multiple individuals to ensure that sex-biased dispersal is not the basis for the species limits proposed.

Operationalizing the telecoupling framework for migratory species using the spatial subsidies approach to examine ecosystem services provided by Mexican free-tailed bats

BackgroundDebate continues as to whether allopatric speciation or peripatric speciation through a founder effect is the predominant force driving evolution in vertebrates. The mouse lemurs of Madagascar are a system in which evolution has generated a large number of species over a relatively recent time frame. Here, we examine speciation patterns in a pair of sister species of mouse lemur, Microcebus murinus and M. griseorufus. These two species have ranges that are disparately proportioned in size, with M. murinus showing a much more extensive range that marginally overlaps that of M. griseorufus. Given that these two species are sister taxa, the asymmetric but overlapping geographic ranges are consistent with a model of peripatric speciation. To test this hypothesis, we analyze DNA sequence data from four molecular markers using coalescent methods. If the peripatric speciation model is supported, we predict substantially greater genetic diversity in M. murinus, relative to M. griseorufus. Further, we expect a larger effective population size in M. murinus and in the common ancestor of the two species than in M. griseorufus, with a concomitant decrease in gene tree/species tree incongruence in the latter and weak signs of demographic expansion in M. murinus.ResultsOur results reject a model of peripatric divergence. Coalescent effective population size estimates were similar for both extant species and larger than that estimated for their most recent common ancestor. Gene tree results show similar levels of incomplete lineage sorting within species with respect to the species tree, and locus-specific estimates of genetic diversity are concordant for both species. Multilocus demographic analyses suggest range expansions for M. murinus, with this species also experiencing more recent population declines over the past 160 thousand years.ConclusionsResults suggest that speciation occurred in allopatry from a common ancestor narrowly distributed throughout southwest Madagascar, with subsequent range expansion for M. murinus. Population decline in M. murinus is likely related to patterns of climate change in Madagascar throughout the Pleistocene, potentially exacerbated by continual anthropogenic perturbation. Genome-level data are needed to quantify the role of niche specialization and adaptation in shaping the current ranges of these species.