© 2007 The Authors
Journal compilation © 2007 The Royal Entomological Society 515
Insect Molecular Biology (2007) 16(5), 515–524 doi: 10.1111/j.1365-2583.2007.00746.x
Blackwell Publishing Ltd
Genetic basis for reproductive diapause is correlated with
life history traits within the Culex pipiens complex
A. Mori, J. Romero-Severson and D. W. Severson
Center for Global Health and Infectious Diseases,
Department of Biological Sciences, University of Notre
Dame, Notre Dame, IN, USA
Abstract
The evolution of late season reproductive arrest
(diapause) among female Culex pipiens mosquitoes
allows them to overwinter in temperate climates, while
females of the sibling species Culex quinquefasciatus
do not exhibit the diapause phenotype. We present
results for quantitative trait loci (QTL) analyses of two
independent segregating populations derived from
crosses between C. pipiens and C. quinquefasciatus.
QTL for diapause and three life history traits were
identified and compared for genome positions and
gene effects. Using a combination of composite interval
mapping, single-marker analysis and all possible
subsets regression, we identified multiple QTL for
each trait, totalling 14 and 17 QTL for each population,
respectively. Individual QTL across traits often mapped
to similar genome locations, suggesting these traits
may be controlled in part by genes with pleiotropic
effects or multiple tightly linked genes. The majority
of QTL were intermediate in magnitude in that they
explained 10–25% of the phenotypic variation. The
majority of QTL showed overdominance effects. We
suggest that this could impact natural populations, as
increased heterosis across hybrid zones may allow
populations to adapt to environmental conditions via
stabilizing selection, and yet maintain species identity
outside these regions because of strong morphological
integration, wherein related traits evolve as an
integrated unit.
Keywords: heterosis, overdominance, photoperiod,
QTL, West Nile virus.
Introduction
Diapause is a state of programmed developmental arrest
that facilitates survival under adverse environmental
conditions. Individuals in diapause exhibit characteristic
changes in morphology, physiology and behaviour com-
pared to nondiapausing individuals (Tauber et al., 1986;
Danks, 1987). Adult diapause is a common adaptation
among some insects for overwintering in temperate climates,
and involves arrested reproductive development, typically
evidenced in females as delayed ovary development
following adult eclosion (Danks, 1987). Diapause status in
receptive individuals is controlled by the interaction between
environmental cues, namely photoperiod and temperature,
and insect hormone activity (Beck, 1980). Short daylength
coupled with low ambient temperatures result in reduced
juvenile hormone secretion by the corpus allatum, which
suppresses reproduction (Denlinger, 1985).
The Culex pipiens complex represents a group of closely
related mosquito species that are distributed nearly world-
wide (Vinogradova, 2000). The major species are delineated
largely by their geographical distribution, with C. pipiens
(identified as C. pipiens pallens in the Far East) largely
associated with temperate zones and C. quinquefasciatus
largely associated with tropical zones. Members of the
C. pipiens complex have been implicated as primary vectors
for the West Nile virus in North America (Fonseca et al.,
2004), and diapausing females can serve as reservoirs for
West Nile virus to re-initiate vertebrate infections in the
spring (Nasci et al., 2001; Farajollahi et al., 2005). Inter-
species hybrids are known to occur in areas where their
distributions overlap (Barr, 1957; Jakob et al., 1979, 1980;
Tabachnik & Powell, 1983; Pryor & Daly, 1991; Cornel
et al., 2003; Fonseca et al., 2004). Investigations of hybrid
zones have confirmed that, although significant introgres-
sion occurs, fitness clines largely related to temperature
gradients are evident (Urbanelli et al., 1995, 1997; Humeres
et al., 1998).
Culex pipiens females are induced into ovarian diapause,
wherein ovarian follicles remain largely undeveloped, by
decreasing photoperiod and low ambient temperatures in
late summer or autumn (Eldridge, 1968; Sanburg & Larsen,
1973). Additionally, females in diapause are characterized
Received 6 December 2006; accepted following revision 5 February 2007;
first published online 17 July 2007. Correspondence: Dr David W. Severson, 137
Galvin Life Sciences, University of Notre Dame, Notre Dame, IN 46556–5645,
USA. Tel.: +1 574 631 3826; fax: +1 574 631 7413; e-mail: severson.1@nd.edu