How Social Structure Drives the Population Dynamics of the Common Vampire Bat (Desmodus rotundus, Phyllostomidae)

Abstract

Social systems are major drivers of population structure and gene flow, with important effects on dynamics and dispersal of associated populations of parasites. Among bats, the common vampire bat (Desmodus rotundus) has likely one of the most complex social structures. Using autosomal and mitochondrial markers on vampires from Mexico, French Guiana, and North Brazil, from both roosting and foraging areas, we observed an isolation by distance at the wider scale and lower but significant differentiation between closer populations (<50 km). All populations had a low level of relatedness and showed deviations from Hardy-Weinberg equilibrium and a low but significant inbreeding coefficient. The associated heterozygote deficiency was likely related to a Wahlund effect and to cryptic structures, reflecting social groups living in syntopy, both in roosting and foraging areas, with only limited admixture. Discrepancy between mitochondrial and nuclear markers suggests female philopatry and higher dispersal rates in males, associated with peripheral positions in the groups. Vampires are also the main neotropical reservoir for rabies virus, one of the main lethal pathogens for humans. Female social behaviors and trophallaxis may favor a rapid spread of virus to related and unrelated offspring and females. The high dispersal capacity of males may explain the wider circulation of viruses and the inefficacy of bat population controls. In such opportunistic species, gene connectivity should be considered for management decision making. Strategies such as culling could induce immigration of bats from neighboring colonies to fill vacant roosts and feeding areas, associated with the dispersal of viral strains.

Temporal patterns of vampire bat rabies and host connectivity in Belize

“…More years of serological data are needed to confirm such patterns, but one explanation for this inverse relationship could be bat movement that causes traveling waves of virus transmission (Bjørnstad et al, 1999). Our microsatellite data suggest historic panmixia of bats in this region of Belize, consistent with low population structure at small spatial scales in Mexico, Peru, and French Guiana, as also inferred using nuclear markers (Romero-Nava et al, 2014;Huguin et al, 2018). Additionally, mark-recapture detected rare but contemporary annual movement between sites, an 8 km distance relative to mean home ranges of 2-3 km (Burns and Crespo, 1975;Trajano, 1996).…”

“…Additionally, use of mitochondrial markers could also help illuminate how sex-dependent behavior shapes virus transmission (Streicker et al, 2016;Huguin et al, 2018). More broadly, however, our results suggest that the degree of connectivity found here likely enables virus persistence through inter-site contacts but is not sufficient to synchronize infection dynamics across sites (Blackwood et al, 2013).…”

“…We assessed fit (R 2 ) using the rsq package (Nagelkerke, 1991). Because male behavior and disperser bias could affect rabies exposure (Streicker et al, 2016;Huguin et al, 2018), we also tested for a correlation between the site-and year-specific fractions of males and seroprevalence.…”

“…To first assess connectivity through bat population genetics, we extracted DNA from wing biopsies (LAR=41, KK=28) using DNeasy Tissue Kits (Qiagen) and amplified nine previously developed nuclear microsatellite loci using a Multiplex PCR Kit (Qiagen; Piaggio et al, 2008). Microsatellites are biparentally inherited markers that have previously captured patterns of vampire bat population structure at both large and fine spatial scales and correlate with patterns of rabies virus spread (Streicker et al, 2016;Huguin et al, 2018). We used Geneious (BioMatters) for microsatellite scoring (Kearse et al, 2012).…”

Evidence for unfamiliar kin recognition in vampire bats

“…The clearest example of kin-biased helping in bats is regurgitated food sharing in vampire bats [17]. Common vampire bats show preferred co-roosting associations with both kin and nonkin (mean within-roost relatedness = 0.08 [18, 19]). Yearling males disperse whereas females are typically philopatric and form long-term cooperative relationships within and between matrilines [17, 20].…”