Bottleneck or founder effect
The haplotype network for ND2 showed the predicted mtDNA starburst
pattern for a population that had experienced a bottleneck or founder
effect, i.e. a star-like shape where core haplotype is shared by most
populations and then many less-common peripheral haplotypes (Ferreri,
Qu, & Han, 2011; inset Figure 3). This result was upheld byTajima’s D , where a negative result indicated a population
expansion after a bottleneck event (Ramakrishnan, Hadly, & Mountain,
2005); for this study we were unable to determine whether this pattern
was due to a bottleneck versus a founder effect. Either instance may be
due to changes in habitat distribution during the last Pleistocene
glacial period —- a possible extrapolation of the Pleistocene refugia
hypothesis (Grubb, 1982). The Pleistocene refugia hypothesis (sometimes
referred to as Holocene Refugia) suggests that repeatedly expanding
glaciers toward the end of the Pleistocene epoch resulted in a large
proportion of speciation events, especially among sister taxa (Avise,
2009; Avise & Walker, 1998). While the Pleistocene refugia hypothesis
has previously undergone criticism stating many of these divergence
events preceded the Pleistocene (Knapp & Mallet, 2003; Whitten, 1979),
there remains a large number of studies across taxa where speciation or
isolation events correlated with major changes in climate
~37 KYA (e.g. Foltz, Nguyen, Kiger, & Mah, 2008;
Johnson & Cicero, 2004; Quick et al., 2016; Ribera & Vogler, 2004;
Vörös et al., 2017).
However, Africa did not have glaciers in the Pleistocene, and so changes
in distribution of C. frenatus were likely due not to glaciers
specifically, but to shifts in vegetation structure from changing
weather patterns during the last glacial period. As the fynbos
experienced a major shift wherein ericaceous fynbos contracted
>96 KYA, expanded ~96–37 KYA, and again
retreated ~37 KYA (Quick et al., 2016), we suggest two
possibilities in relation to this hypothesis: (1) C. frenatus may
have been confined to one mountain range when fynbos retreated
>96 KYA, then radiated out from this bottleneck population
when fynbos expanded ~96–37 KYA; or (2) C.
frenatus was extirpated (or not initially present) in the Cape Fold
Belt, but the expansion of ericaceous Fynbos ~96–37
KYA, along with shrinking surrounding Afromontane forests, leading to
colonisation by a founder population of the sister C. aurantiuslineage. In the second scenario, speciation may have been promoted by
geographic isolation resulting in the current differences between the
two species. However, the bottleneck or founder population of C.
frenatus may also have originated much earlier during the Miocene, as
Cape Fold uplift during this time period has been suggested as the main
source of speciation among fynbos plant communities (Cowling, Procheş,
& Partridge, 2009; Pirie et al., 2016).
From a purely genetic perspective, our results suggest C.
frenatus and C. aurantius have low species-level diversity based
on uncorrected p -distance values. Our recorded cytbp- distance result for C. frenatus -C. aurantius (1.5
%) was below most p -distance values for species-level distances
of 3.3–12.8 % in passerines (Liu et al., 2016; Luo et al., 2014;
Martens, Tietze, & Sun, 2005), although (Martens, Tietze, & Päckert,
2011) suggested sister-species can be <3 %. Similarly, our
recorded ND2 p -distance result for C. frenatus -C.
aurantius (4.3 %) was at the lower range of p -distance values
for previous species-level distances of 2.0–13.7 % of passerines
(Aliabadian et al., 2012; Luo et al., 2014; Zuccon & Ericson, 2012).
However, this is not entirely surprising, as (Martens et al., 2011)
indicate one should use caution in applying previous speciesp -distance values to apparent sister species.
Edge extinction
The mountain Fynbos of South Africa extends from the coast of the Cape
Peninsula (in the very southwest corner of South Africa), to
~300 km north into the Cederberg mountains, and
~600 km east ending near Port Elizabeth. Thus, while the
Cape Peninsula consists of habitat which is suitable forC. frenatus , there have been no records of birds on these
mountains in recorded history (Cohen and Frauenecht 1993); indeed, there
are also no records from the eastern coastal edges of mountain fynbos
habitat (Lee & Barnard, 2016). Species extinction is often preceded by
initial habitat fragmentation and increasing distance between suitable
patches, resulting in local population extinction on the edges of a
species distribution (Ceballos & Ehrlich, 2002; Woodroffe & Ginsberg,
1998). Conceivably C. frenatus were once located in this area,
but have since been extirpated. This may have been due to human
encroachment (or human-associated species such as domestic cats and
dogs, or invasive rats) or the area became unsuitable due to too many
years between fires. In the first instance, it may be that C.
frenatus do occasionally recolonize the mountains only to be again
driven off by anthropogenic disturbance, and in both instances it may be
that once C. frenatus edge territory populations become extinct
they are unlikely to recolonize [as suggested by Ceballos and Ehrlich
(2002)]. Such edge extinction may have occurred as recently as the
last three decades as despite seemingly suitable habitat on the Lady
Slipper mountain range near Port Elizabeth, Eastern Cape, where birds
were recorded by SABAP1 (1987 - 1991), there are no records from the
more recent SABAP2 (2007 to present).
Increased variation at the edge of species’ distributions has been
attributed to reduced dispersal and gene flow (Sittenthaler et al.,
2018), fragmentation, isolation, genetic drift, and small population
size (Arnaud‐Haond et al., 2006; Böhme, Schneeweiß, Fritz, Schlegel, &
Berendonk, 2007), or human conflict (Woodroffe & Ginsberg, 1998). In
addition, while samples collected from the furthest east known
occurrence of C. frenatus in 2017 (i.e. Kleinrivier), none were
recorded on return in 2019 (pers. obs. KNO). As in Black GrouseTetrao tetrix (Sittenthaler et al., 2018), the greatest genetic
variation for C. frenatus was found in edge populations (i.e.
Kogelberg; inset Figure 3). In all cases, these edge populations are
placed at increased risk of extinction (Ceballos & Ehrlich, 2002;
Woodroffe & Ginsberg, 1998).
Conclusions
Genetic theory predicts reduced effective population size will result in
a substantial loss of genetic variation, corresponding to a reduction in
allele number and heterozygosity at polymorphic loci (Nei, 1978; Varvio,
Chakraborty, & Nei, 1986). It thus seems possible that decliningC. frenatus populations are resulting in an overall loss of
genetic diversity, although low diversity may also be due to selective
pressure. While we did not detect any geographical genetic structure inC. frenatus populations, their overall low genetic diversity
suggests further research is needed to conserve remaining populations
and dispersal avenues. Moreover, as C. frenatus habitat continues
to warm, and suitable alpine Fynbos retreats upslope, it seems likely
climate change will impact gene flow in the future. Our finding of low
genetic variation and no genetic structuring may be complicated by the
specialized niche inhabited by C. frenatus ; that being said, a
lack of genetic diversity may indicate an inability to adapt to changing
environments. The signature of a bottleneck/founder effect withinC. frenatus suggests an interesting link between paleoclimate,
the potential for climate refugia, and current species distributions in
the Fynbos. While this is the first genetic structuring study on an
avian endemic of the Cape Fold Belt sky islands, our study provides
insights into processes that may have impacted speciation and evolution
within this unique study system.