Successfully invasive species are often characterized by their ability to quickly colonise new habitats. In some cases, however, otherwise successful invasive species spread more slowly than we might expect. Why?
Such is the case with the Asian honey bee, Apis cerana in Far North Queensland Australia. This honey bee was introduced accidently to the region in 2007, where it established and spread despite eradication efforts. Today the population numbers tens of thousands of colonies, but available data suggests this all stemmed from just a single founding colony (one mated queen and her workers). It’s therefore not surprising that the population has very low genetic diversity, relative to Apis cerana populations back in Asia.
Such a stark founding bottleneck for honey bees comes with severe consequences, as bees have a sex determination system that relies on populations having high allele number at a critical “sex locus”. Embryos heterozygous at this locus become healthy females, while embryos homozygous at the locus do not survive. This begs the question, how do honey bees survive such intense bottlenecks? In 2017, our lab answered this mystery using time-series data of allele frequencies at the sex locus: (https://communities.springernature.com/posts/honey-bee-invaders-show-us-balancing-selection-in-action): allele diversity at the sex locus of invasive Apis cerana was indeed low, but not as low as it could be thanks to the action of strong negative-frequency-dependent selection. This balancing selection prevented the loss of rare alleles and corrected the initial skew in allele frequency in the years post-invasion to minimize genetic load. A seemingly textbook example then of the impact balancing selection had on populations in real time, but we were left with some questions. Above all, we noticed the population, though growing exponentially in size, was spreading outwards at a pretty modest rate. This is despite the fact that the habitat to the north and south of the invasion seems ideal for tropical honey bees. Another mystery for us to solve.
We reasoned that the same allele frequency skew at the sex locus (and corresponding high genetic load) that had occurred during the initial founder event (i.e. the colonization of Australia) might also be occurring with each “serial founder event” as the population expanded outward (i.e. small numbers of colonies extending beyond the current range). We set out then to investigate spatial variation in sex locus allele frequencies across this population, via three lines of evidence. First, we found the frequency of sex alleles at different regions of the invasive range (including centre and edges) by collecting thousands of males (drones) at honey bee mating congregations. Second, we collected colonies from across the range to assess whether differences in local sex allele frequencies resulted in corresponding differences in brood survival. Finally, we developed a model that simulated an invasive social insect population with a homozygous-lethal sex locus, to see if we could consistently replicate real world results. Together, these triplicate lines of evidence gave us our answer. Near ranges edges, the population had significantly reduced sex locus diversity and significantly lower rates of brood survival per colony than populations at the range centre. This result is consistent with populations near range edges experiencing repeated serial founder effects. Moreover, these serial founder effects could explain a slower-than-expected expansion rate. Using our simulation, we modelled populations without and without genetic load at the sex locus and found that those incurring this range edge load spread less quickly.
Our study adds to the growing body of research that highlights the importance of studying populations in motion to better understand the diverse eco-evolutionary processes that may impact invasive species beyond selection alone (other examples being mutation surfing and phenotypic sorting).
So, what is the fate of Australia’s invasive Apis cerana? Without genetic rescue in some capacity, either via the introduction of new sex alleles from source populations and/or by mutation, the population is likely to continue to grow, but inching rather than bounding outwards due to the combination of low genetic diversity and ongoing founder effects at range edges.