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\begin{document}

\title{Divergent island hybrids mixing waves of ancient gene flow}



\author[1]{Silu Wang}%
\affil[1]{University at Buffalo}%


\vspace{-1em}



  
  \date{June 13, 2024}


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\selectlanguage{english}
\begin{abstract}
In this issue of Molecular Ecology, Salter et al. (2023) discovered that
the Cuban Northern Bobwhite subspecies, Colinus virginianus cubanensis
(Gould, 1850), is an ancient hybrid population formed due to historical
hybridization between lineages from divergent spatiotemporal origins.
Slater et al. sequenced genomes extracted from contemporary samples of
Northern Bobwhites, as well as historical museum specimens with the
oldest specimens dated in 1859. With this data, they reconstructed the
evolutionary origin and history of C.v. cubanensis by combining
historical literature with demographic modeling. The demographic model
revealed the hybrid origin of the C.v. cubanensis from hybridization
between divergent lineages. The Bobwhite first arrived in Cuba between
the 12th and 16th centuries from Southern Mexico. Then the secondary
gene flow from the Southeastern USA occurred between the 18th and 20th
centuries (Figure 1). C.v. cubanensis are hybrids with mixed ancestries
while possessing unique genetic variants, which confirm the subspecies
status. Hybridization can be a creative process generating and
maintaining genetic diversity over space and time.%
\end{abstract}%



\sloppy


\textbf{Divergent island hybrids mixing waves of ancient gene flow}

Silu Wang

Department of Biological Sciences, University at Buffalo

109 Cooke Hall, North Campus, Buffalo, NY 14260, U.S.A.

\textbf{In this issue of Molecular Ecology, Salter et al. (2023)
discovered that the Cuban Northern Bobwhite subspecies,} \emph{Colinus
virginianus cubanensis} (Gould, 1850), \textbf{is an ancient hybrid
population formed due to historical hybridization between lineages from
divergent spatiotemporal origins.} Slater et al. sequenced genomes
extracted from contemporary samples of Northern Bobwhites, as well as
historical museum specimens with the oldest specimens dated in 1859.
With this data, they reconstructed the evolutionary origin and history
of \emph{C.v. cubanensis} by combining historical literature with
demographic modeling. The demographic model revealed the hybrid origin
of the \emph{C.v. cubanensis} from hybridization between divergent
lineages. The Bobwhite first arrived in Cuba between the
12\textsuperscript{th} and 16\textsuperscript{th} centuries from
Southern Mexico. Then the secondary gene flow from the Southeastern USA
occurred between the 18\textsuperscript{th} and
20\textsuperscript{th}centuries (Figure 1). \emph{C.v. cubanensis} are
hybrids with mixed ancestries while possessing unique genetic variants,
which confirm the subspecies status. Hybridization can be a creative
process generating and maintaining genetic diversity over space and
time.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

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\textbf{Figure 1} \textbf{A Brief History of Northern Bobwhites} . Left:
illustration (Pope, 1878) of a Northern Bobwhite (\emph{Colinus
virgnianus} ) breeding pair and the fledglings. Right: the
reconstruction of historical gene flows that gave rise to \emph{C. v.
cubanensis} based on Slater et al. (2023). Map illustration by Wang S.
with the reference of \emph{C. virgnianus} range map from BirdLife
International (2016).

\emph{A complex evolutionary history}

Salter et al. (2023) carefully combined historical literature with
demographic modeling to reconstruct the backbone of the evolutionary
history of the Cuban Northern Bobwhites. Despite that there was
uncertainty in the timing and frequencies of the earlier colonization
events, the model confidently showed: (1) the divergence among
Southeastern U.S., Northern and Southern Mexican populations occurred
around 300 Kya; and (2) that the initial Cuban colonization was from
Southern Mexico and the secondary gene flow was from Southeastern USA.

The timing of the initial arrival provides clues for whether the
founding event was human-mediate or not. The initial migration from
Southern Mexico to Cuba could be aided by the lower sea level without
human mediation 5 kya. However, if the initial colonization date is much
more recent (\textless{}0.5 Kya) when the sea level has become much
higher, human mediation would be more necessary. Unfortunately, the
demographic models could not discern these two possibilities. I wonder
if a model with two gene flow pulses from Southern Mexico would fit the
data better after controlling for the extra migration parameter.

Reconstructing ancient gene flow events is generally challenging when
evaluating demographic models with limited subsamples from contemporary
populations, which might not sufficiently represent the target
populations. Moreover, small, isolated populations that are subject to a
greater extent of gene drift might rapidly lose many ancestral variants
that had contributed to the initial admixture. The Southern Mexico
source population is also isolated from other Bobwhite populations by
the Gulf of Mexico and the Transvolcanic Belt. Therefore, both the
source and the island population could be subject to rapid loss of
ancestral variants due to drifts after the ancient gene flow. Luckily,
this study had historical samples that contributed resolution closer to
the ancient gene flow event(s), empowering its reconstruction. This
allows the model to confidently estimate the historical gene flow from
the Southeastern USA. However, the date of the initial arrival to Cuba
from Southern Mexico was still uncertain. The ancient evolutionary
history is apparently beyond the limit of the demographic models.

\emph{Asymmetry of Introgression}

The asymmetric admixture in \emph{C. v. cubanensis} is remarkable. The
Southeastern USA ancestry is four times more prevalent than the Southern
Mexican ancestry in \emph{C. v. cubanensis} . Introgression sustains and
rescues populations from drift load by masking the deleterious alleles
(MacPherson et al. 2023). This asymmetry indicates the relatively
greater genetic load in the Cuba versus Southeastern USA populations at
the time of hybridization. The isolated Cuban island population could
have been susceptible to receiving foreign alleles from recent gene
flow. This Cuban population that received historical introgression but
still harbors its unique alleles could provide valuable insight for
assisted gene flow programs for wildlife conservation.

\emph{Divergent hybrids in the changing world}

Divergent ecoclimatic adaptation may drive the divergence of hybrid
populations from the parental populations if divergently adapted
parental lineages hybridized and recombined in a novel ecoclimatic
environment. The Cuban bobwhites reside in a distinct ecoregion (the
West Indies) than its parental lineages (Tropical Wet Forest and Eastern
Temperate Forest). This resembles the ancient hybrid
\emph{Setophaga}warblers in coastal North America that contain locally
adapted genetic variants and reside in a climatic condition distinct
from the parental ranges (Wang et al. 2021). We might be only seeing the
tip of the iceberg of the divergent ancient hybrid populations due to
the prehistoric shifts in population ranges driven by the changing
ecoclimatic conditions. Future studies could investigate whether the
unique variants and/or the unique combinations of parental variants are
selected for ecoclimatic adaptation.

\emph{Naturalized anthropogenic hybrid populations}

Should \emph{C. v. cubanensis} lose its conservation attention because
of its hybrid origin? I would argue not. \emph{C. v. cubanensis} harbors
an equivalent amount of unique genetic variants as the Southern Mexican
population and thus contributes to the valuable genetic diversity of the
nearly threatened species. Since the initial arrival to Cuba 0.5-5 Kya,
the Cuban ecological community has been coevolving with this terrestrial
bird. The absence of this species might perturb the ecosystem. \emph{C.
v. cubanensis} is thus a naturalized anthropogenic hybrid population
that contributes to local biodiversity. This study shed light on
historical human migration in shaping the biodiversity around the world.

\textbf{Reference}

BirdLife International. 2016. Colinus virginianus. The IUCN Red List of
Threatened Species 2016: e.T22728956A95000808.
https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22728956A95000808.en.
Downloaded on 27 June 2018.CC BY-SA 4.0

Gould, J. (1850). A monograph of the Odontophorin\selectlanguage{ngerman}æ, or, Partridges of
America. John Gould, F. R. S. Preface {[}a monograph of the
Odontophorinæ, or, partridges of America{]}.

MacPherson A., Wang S., Rieseberg L., Yamaguchi R., Otto S. 2022.
Parental population~range expansion before secondary contact promotes
heterosis.~American Naturalist. 200: E1-E15.

Pope., A. Jr. 1878. Part third, plate V, in: Upland game birds and
waterfowl of the United States. Charles Scribner's Sons, New York,
United States.

Slater J.F., Brumfield, R.T., Faircloth, B.C. 2023. An island `endemic'
born out of hybridization between introduced lineages. Mol. Ecol.
00:1-15.

Wang S., Ore M. Mikkelsen E., Lee-Yaw, J., Rohwer S., Irwin DE. 2021.
Signatures of mito-nuclear climate adaptation in a warbler species
complex.~Nature Communications. 12:4279.\selectlanguage{english}
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