Kleptoparasites of social spider colonies do not track hosts' subdivided population structure.

Abstract

Organisms with lower dispersal abilities tend to have more genetically dissimilar populations. The same is true for parasites, whose transmission frequency may depend on the population structure of the host. This should be especially true when hosts and parasites face similar barriers to dispersal. Here, we considered the similarities between host and parasite population structure in a social spider system. In this system, host colonies are typified by rapid growth via internal recruitment followed by budding or fission events when colonies grow too large, with each colony representing a distinct population. Host colonies provide habitat for kleptoparasitic spiders, which steal prey from and may also feed directly on host individuals. We asked whether kleptoparasites exhibit a similar degree of population subdivision as their host. Under the free-mixing hypothesis (i.e., horizontal transmission), kleptoparasites would have well-mixed populations across broader regions than a single host nest, whereas host populations would be strongly genetically structured. Under the host-tracking hypothesis (i.e., vertical transmission), kleptoparasites would have a population structure that parallels that of the host. We conducted a genotype-by-sequencing study to assess the population structure of both hosts and kleptoparasites within three nearby regions in eastern Ecuador. We found strong signatures of population differentiation and bottlenecks in the host species, which is congruent with past studies. However, we found that kleptoparasite populations were well mixed across host nests, with no evidence of recent bottlenecks. These results support our free-mixing hypothesis, suggesting that kleptoparasites follow patterns of horizontal transmission in this social spider system.