Replicate hybrid zones suggest a limited role of plumage in
reproductive isolation among subspecies of the Variable Seedeater
(Sporophila corvina)
Running title: Limited role of plumage in hybridization
Diego Ocampo1,2,3*, Kevin Winker4,
Matthew J. Miller3,4,5, Luis
Sandoval6, J. Albert C. Uy2
- Department of Biology, University of Miami, Coral Gables FL 33146, USA
- Department of Biology, University of Rochester, Rochester, NY 14627,
USA
- Smithsonian Tropical Research Institute, 0843-03092 Balboa, Ancon,
Panama
- University of Alaska Museum, 907 Yukon Drive, Fairbanks, AK 99775, USA
- Reneco International Wildlife Consultants, Abu Dhabi, UAE
- Laboratorio de Ecología Urbana y Comunicación Animal, Escuela de
Biología, Universidad de Costa Rica, 11502 San José, Costa Rica.
KEYWORDS: genetic divergence, hybridization, plumage coloration,
replicated contact zones, secondary contact.
Contact zones between hybridizing taxa offer a window into the
speciation process (Barton & Hewitt, 1985; Harrison, 1990; Price,
2008). For instance, contact zones shed light on which traits are
important for assortative mating and reproductive isolation, as well as
the genomic basis of such traits (Barton & Gale, 1993; Nadeau et al.,
2014; Semenov et al., 2017). Hybridization between differentiated taxa
may have different outcomes (Abbott et al., 2013), such as the merger of
distinct lineages (Todesco et al., 2016), or even the rise of a new and
independent lineage through homoploid hybrid speciation (Mavárez &
Linares, 2008). However, the degree of the homogenization is dependent
on the biology of the taxa involved (Gompert et al., 2017; Irwin &
Schluter, 2021). Identifying the factors that promote or limit gene flow
among divergent populations is key to uncovering the origin of
reproductive barriers, and thus the drivers of speciation (Coyne & Orr,
2004; Jiggins & Mallet, 2000).
Characterizations of hybrid individuals and hybrid zones offer further
insights into the dynamics shaping interactions among lineages. For
instance, comparisons of hybrid indices, which estimate the proportion
of an individual’s ancestry from different lineages, and the level of
heterozygosity at well-differentiated loci can classify individuals as
first-generation hybrids, later-generation hybrids, or backcrosses
(Fitzpatrick, 2012). Moreover, geographic clines provide insight into
the role of deterministic processes in maintaining species boundaries,
by fitting clinal models of how traits and genetic markers transition
between distinctive populations (Endler, 1977). Here, the width of the
cline provides a measure of the permeability of the reproductive
barrier, and the concordance between cline widths of different traits
can inform about the relative strength of selection on a given trait
(Barton & Gale, 1993). Further, comparing cline centers may identify
traits and genes that have undergone differential introgression (e.g.,
Baldassarre et al., 2014; Brumfield et al., 2001). Overall, these
characterizations offer insights into which traits are important in
causing reproductive isolation, the strength of selection on different
traits, and even the relative fitness of individuals with mixed ancestry
(e.g., Coster et al., 2018; Walsh et al., 2016).
Interpreting contact zone dynamics is often challenging, as the same
pattern of phenotypic and genetic variation can result from different
processes (Harrison, 1990). For example, an intergradation between two
divergent populations might have occurred from ongoing parapatric
divergence (i.e., primary contact) or from hybridization after
differentiation in geographic isolation (i.e., secondary contact;
Morales-Rozo et al., 2017). Comparing model support of alternative
demographic scenarios based on coalescent theory may differentiate
primary versus secondary contact, thus providing better estimates of
important demographic parameters, such as rates and timing of gene flow,
that have created the observed patterns of genomic variation (Marchi et
al., 2021). Characterizing the situation at replicated hybrid zones
increases the power and resolution to infer the factors driving
divergence and introgression, because parallel results increase the
support and likelihood for a given interpretation (Nadeau et al., 2014)
and different results can help to distinguish independent effects of
different factors shaping hybrid zone dynamics (Scordato et al., 2020).
The Variable Seedeater (Sporophila corvina ) is a small tanager
species which consists of four subspecies demonstrating relatively low
genetic differentiation yet substantial phenotypic divergence (Ocampo et
al., 2022a). Three subspecies occur in relatively close proximity across
Costa Rica and Panama. The nominate subspecies S. c. corvina has
almost completely black plumage and is distributed along the Caribbean
slope from northeastern Costa Rica through central Panama. The other two
subspecies, S. c. hoffmanni and S. c. hicksii, have white
collars, bellies, and rumps (a pied plumage), differing only on the
extent of the white patch of the throat (Olson, 1981), and range along
the Pacific slope from central Costa Rica to eastern Panama. The species
is absent in the high-elevation mountain ranges that separate the
Caribbean and Pacific lowlands of Costa Rica and western Panama, but the
three subspecies have contact where their distributions overlap. The
three contact zones are as follows. First, previous morphological
studies addressing taxonomic limits and distributions in this species
have characterized a hybrid swarm occurring between S. c. corvinaand S. c. hicksii in central Panama (Hellmayr, 1938; Olson, 1981;
Stiles, 1996; Figure 1A, no. 1), while the contact zone between S.
c. hoffmanni and S. c. hicksii is less clearly understood as an
intergradation of these subspecies at the Pacific slope in Veraguas
province, based on a few specimen records of intermediate phenotypes
(Olson, 1981; Figure 1A, no. 2). Finally, recent observations in the
Central Valley of Costa Rica suggest the existence of a third contact
zone between populations of S. c. hoffmanni and S. c.
corvina (examples of observations available at eBird: www.ebird.org;
Figure 1A, no. 3). This final contact zone might have been mediated by
deforestation and urbanization in Costa Rica over the last few decades
(Joyce, 2006), creating artificial corridors that could have facilitated
interbreeding between previously isolated clades (Carantón‑Ayala et al.,
2018; Moulton et al., 2017). However, these contact zones and
interactions between subspecies are poorly studied, and to date, little
is known about the genetic consequences of these three independent
contact zones.
Here, we take advantage of the replicate contact zones between
subspecies pairs of S. corvina occurring in Costa Rica and Panama
(Figure 1A), looking at the fine-scale genetic variation and structure
between populations and subspecies, to evaluate the role of phenotypic
divergence and ecological barriers in mediating gene flow. We evaluate
how differences in morphology and plumage pattern covary with genomic
divergence to test the hypothesis that differentiation in plumage color
is an important signal for conspecific recognition and thus acts as a
reproductive barrier. We expect lower genomic differentiation and higher
rates of hybridization between phenotypically similar subspecies (i.e.,S. c. hoffmanni and S. c. hicksii ) than more
phenotypically divergent subspecies (e.g., S. c. corvina andS. c. hicksii ). Moreover, we characterize genomic hybrids and
hybrid zones, and use model-based demographic inference to infer the
most likely evolutionary scenarios shaping current patterns of genomic
admixture and differentiation between subspecies.
METHODS