Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Abstract

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin-structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long-term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female-biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine-scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine-scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female-biased dispersal alone is unlikely to be an effective strategy.

Variation in fine‐scale genetic structure and local dispersal patterns between peripheral populations of a South American passerine bird

“…Separate spatial autocorrelation analyzes were performed for each sex/population (Nav: 82 females, 79 males; FJ: 69 females, 66 males) based on all genotyped individuals for 2010-2015 (e.g., Van Dijk et al, 2015). We repeated the same analyzes on "snapshot" years to check for possible temporal sampling effects due to demographic processes (Foerster, Valcu, Johnsen, & Kempenaers, 2006;Van Dijk et al, 2015),…”

“…Fine-scale genetic population structure arises when alleles or genotypes are nonrandomly distributed across space. This is typically a consequence of the interaction between environmental heterogeneity and species-specific life history traits such as dispersal patterns, mating systems, and demography (Garroway et al, 2013;Greenwood & Harvey, 1982;Lee, Simeoni, Burke, & Hatchwell, 2010;Van Dijk, Covas, Doutrelant, Spottiswoode, & Hatchell, 2015;Woxvold, Adcock, & Mulder, 2006). Even though mobile organisms such as birds are expected to show high levels of gene flow within and among populations, spatial genetic structure has been detected in a wide variety of species with differing dispersal abilities and social organization (e.g., Beck, Peakall, & Heinsohn, 2008;Browne, Collins, & Anderson, 2008;Klauke, Schaefer, Bauer, & Segelbacher, 2016;Lee et al, 2010;Pierson, Allendorf, Saab, Drapeau, & Schwartz, 2010;Temple, Hoffman, & Amos, 2006).…”

“…Several studies focusing on the influence of habitat heterogeneity on gene flow have investigated spatial variation at the landscape level (>10 km), and detected genetic differences among populations of species that showed high habitat specificity (e.g., Browne et al, 2008;Walsh, Kovach, Babbit, & O′Brien, 2012;Woltmann, Kreiser, & Sherry, 2012) or sex-biased and/ or restricted dispersal (e.g., Coulon, Fitzpatrick, Bowman, & Lovette, 2010;Coulon et al, 2008;Hermes, Döpper, Schaefer, & Segelbacher, 2016;Pierson et al, 2010). On the other hand, studies aiming at linking spatial patterns to complex social interactions have assessed genetic variation at a smaller geographic scale (<5 km), and found finescale genetic structure within populations of cooperatively breeding and lekking birds (e.g., Beck et al, 2008;Double, Peakall, Beck, & Cockburn, 2005;Van Dijk et al, 2015).…”

“…Although complex social interactions are viewed as a main driver of fine-scale genetic structure within local populations of birds (Hatchwell, 2009;Van Dijk et al, 2015), environmental heterogeneity can also affect the distribution of individuals at small spatial scales (Lindsay et al, 2008), especially if nonmigratory movements are restricted by habitat patchiness (Harris & Reed, 2002). Natal and breeding dispersal can be severely limited even if there are only relatively small gaps between patches of suitable habitat.…”

“…As variability in habitat patchiness and population density can affect local gene flow (Walsh et al, 2012), distinct patterns of finescale genetic structure between breeding populations are likely to occur (Hermes et al, 2016;Lee et al, 2010;Stow, Sunnucks, Briscoe, & Gardner, 2001). However, the mechanisms behind within-species variation in dispersal patterns and in microgeographic genetic structure and the effects of varying life histories or contrasting ecological conditions remain relatively poorly understood (Le Galliard, Massot, & Clobert, 2012;Van Dijk et al, 2015).…”