Divergence, admixture and speciation
The role of climate fluctuations in causing secondary contact of
recently diverged species is well known (Hewitt 1999), with the outcomes
varying from free admixture, to directional gene flow, to complete
isolation or even hybrid speciation. Several cases demonstrating the
range of these outcomes are known from alpine taxa within the Sierra
Nevada Mountains (Gompert, Fordyce, Forister, Shapiro, & Nice, 2006;
Rovito 2010; Rubidge, Patton, & Moritz, 2014). The degree and
geographical scale of admixture likely varies across taxa due to a
number of factors, including the dispersal ability of species, habitat
suitability and connectivity, as well as the reproductive compatibility
of lineages and fitness of hybrids (Barton & Hewitt 1985; Dufresnes,
Berroneau, Dubey, Litvinchuk, & Perrin, 2020).
In this study, we found that an intermediate morphotype in the N.
ingens complex (Schoville et al. 2012) extends to populations
throughout the Central Sierra Nevada, encompassing the entire San
Joaquin drainage and extending south to contact zones in the Kings River
watershed (sites 14 and 15; Figure 1 ). The distribution of the
morphological phenotype is different from the observed genetic patterns,
where mitochondrial haplotype variation suggests introgression fromN. riversi into nearly the entire southern range of N.
ingens (Figure 2 & S2 ), and genome-wide nuclear markers
suggest that the intermediate morphotype is an independent lineage (site
9, 10 and 12; Figure 3 ). For example, in the sNMF analysis
(from K=3 to K=11), most individuals representing the intermediate
morphotype do not show extensive ancestry from either N. riversior N. ingens (Figure S1 ). Additionally, TMRCA estimates
between populations of the intermediate morphotype and either species
mostly predate the last glacial maximum. Despite this genetic
divergence, we found no evidence of premating isolation among the three
lineages (Table 3 ), although our sample sizes were low.
Based on these results, we infer that 1) an early glacial cycle caused
deep divergence to form between northern and southern populations, which
formed N. ingens and N. riversi . In a subsequent glacial
cycle, 2) a contact zone formed near the San Joaquin drainage and led to
the formation of the intermediate morphotype. This lineage diversity was
maintained during the last glacial maximim and 3) allowed for the
formation of more complex population structure as each major lineage
recolonized high elevation habitat. It is clear that limited gene flow
occurs in parts of the alpine range, leading to the formation of a
genetic cline in genetic divergence measures such asF ST. The general pattern we observe is consistent
with models of diversification linked to the orbitally forced range
dynamic (ORD) model (Dynesius & Jansson, 2000), and the more recently
coined ’mix-isolation-mix’ model proposed by He et al. (2019).