Abstract
Genetic analyses of speciation have focused nearly exclu-
sively on retrospective analyses of reproductive isolation
between highly divergent species. Yet, a full understanding
of the speciation process must encompass analysis of the
consequences of genomic divergence in young lineages still
capable of exchanging genes under natural conditions. The
accumulation of conditionally neutral genetic variation may
lead to the evolution of divergent gene networks. In a hybrid
background, such mutations may no longer compensate one
another, resulting in the appearance of selectively disadvan-
tageous traits, including disruption of gene expression
regulation. Here, we documented genome-wide patterns of
gene expression divergence between young lineages of
normal and dwarf lake whitefish and their backcross hybrids
for which strong, yet incomplete post-zygotic isolation
barriers exist. A significant proportion (33%) of backcross
hybrids showed developmental abnormalities not seen in
parental forms and eventually leading to death. Although the
transcriptome of parental forms was nearly identical during
embryonic development, suggesting a role for stabilizing
selection, all hybrids displayed strongly divergent patterns of
gene expression. By comparing healthy, surviving hybrids
against moribund ones showing abnormal development, we
observed that over 2000 genes were misregulated in these
abnormal embryos. In particular, misregulation was signifi-
cantly biased toward essential developmental genes, which
were severely underexpressed. Furthermore, genes pre-
viously documented to be highly transgressive (exaggerated
inter-individual variance) were almost invariably under-
expressed in hybrids. Our results thus clearly showed a
transcriptome-wide signature of hybrid breakdown in young,
incipient species and demonstrated a persuasive link
between misexpression of essential developmental genes
and post-zygotic isolation.
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