Species delimitation and dispersal capabilities within the C.
variipennis complex
The high degree of genetic differentiation between clusters inferred by
the SNP data supports the current species groupings of the C.
variipennis complex (C. occidentalis , C. sonorensis , andC. variipennis ), as well as raising C. albertensis and a
cryptic species in San Diego, California to species status. Little to no
IBD or structure was found within populations of C. albertensis ,C. sonorensis , and C. variipennis (Fig. 3a,c,d). The
number of populations inferred by fastSTRUCTURE for C. sonorensiswas K=2; however, a mean pairwise FST of 0.0287
suggests that a high amount of gene flow still exists between all
populations. This could also be an artifact of the propensity of delta K
inferring two populations (Janes et al., 2017) or from a high level of
relatedness among individuals from KS.
Interestingly, although no IBD was found in C. occidentalis , each
location of this species clustered as a distinct population. The lack of
IBD is therefore not indicative of a single, genetically homogeneous
population, but rather stems from high levels of divergence between
populations regardless of their geographic distances. In this species,
the strong genetic divergence between the population from California and
the other populations observed in the SNP data was consistently
uncovered in the mtDNA (4.0% divergent, Table 3, Fig. 5). It is
possible that this may represent a further cryptic species with a
dispersal barrier created by the Sierra-Nevada mountain range.
Patchiness of the larval habitat of C. occidentalis could also
create isolation between populations as well as reduce the number of
individuals within each population. A small population size with little
to no immigration would allow for a strong effect from drift (Hare,
2001). While the populations of C. occidentalis outside of
California were less diverged from one other, the lowest pairwiseFST values between these populations were still
greater than the highest pairwise values observed for any other species,
consistent with the findings of Holbrook et al. (2000) (Table 2).
Interestingly, at one of the three loci found to be under selection with
the complex (seipin, Table S4), all populations of C.
occidentalis and C. albertensis were fixed for a single allele,
whereas the other three other species were fixed for the other
alternative allele. This SNP was determined to be synonymous and
therefore unlikely to be the direct target of selection; however, it may
be linked to a region of the genome that is.
Similar to other species of Culicoides (Jacquet et al., 2015;
Mignotte et al., 2021; Onyango, Beebe, et al., 2015; Onyango, Michuki,
et al., 2015), high values of the inbreeding coefficient were
observed in all species investigated in this study (Table S2). Although
these previous studies have suggested that the observed high inbreeding
coefficient values are an artifact from a large number of null alleles,
the consistent reporting of these findings across various species using
several types of molecular markers lends support to the they hypothesis
that high inbreeding has a biological origin. High levels of inbreeding
and heterozygote deficiencies are common among mosquitoes (Fonseca,
Smith, Kim, & Mogi, 2009; Goubert, Minard, Vieira, & Boulesteix, 2016;
Lehmann et al., 1997), even when using markers with a low level of null
alleles (Chapuis & Estoup, 2006; Manni et al., 2015). Goubert et
al . (2016) considered the typical Aedes albopictus population as
“a network of interconnected breeding sites, each with a high level of
inbreeding”. In this study, although we cannot rule out that the
presence of null alleles and we acknowledge that a weak Wahlund effect
can contribute to the level of inbreeding, our results strongly
suggested that some aspects of the reproductive biology ofCulicoides induce inbreeding within populations.