Limits...
Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

McBride CS, Singer MC - PLoS Biol. (2010)

Bottom Line: We then conducted field experiments to estimate the effects of intermediacy on fitness in nature.Our results revealed strong EPI under field conditions.Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females.

View Article: PubMed Central - PubMed

Affiliation: Center for Population Biology, University of California Davis, Davis, California, USA. lmcbride@rockefeller.edu

ABSTRACT
Gene flow between populations that are adapting to distinct environments may be restricted if hybrids inherit maladaptive, intermediate phenotypes. This phenomenon, called extrinsic postzygotic isolation (EPI), is thought to play a critical role in the early stages of speciation. However, despite its intuitive appeal, we know surprisingly little about the strength and prevalence of EPI in nature, and even less about the specific phenotypes that tend to cause problems for hybrids. In this study, we searched for EPI among allopatric populations of the butterfly Euphydryas editha that have specialized on alternative host plants. These populations recall a situation thought typical of the very early stages of speciation. They lack consistent host-associated genetic differentiation at random nuclear loci and show no signs of reproductive incompatibility in the laboratory. However, they do differ consistently in diverse host-related traits. For each of these traits, we first asked whether hybrids between populations that use different hosts (different-host hybrids) were intermediate to parental populations and to hybrids between populations that use the same host (same-host hybrids). We then conducted field experiments to estimate the effects of intermediacy on fitness in nature. Our results revealed strong EPI under field conditions. Different-host hybrids exhibited an array of intermediate traits that were significantly maladaptive, including four behaviors. Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females. We used our empirical data to construct a fitness surface on which different-host hybrids can be seen to fall in an adaptive valley between two peaks occupied by same-host hybrids. These findings demonstrate how ecological selection against hybrids can create a strong barrier to gene flow at the early stages of adaptive divergence.

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Summary of traits addressed in this study.E. editha populations adapted to Collinsia torreyi (top row) and Pedicularis semibarbata (bottom row) have diverged in the six traits illustrated—two expressed in larvae and four expressed in adult females [40]. Larval performance: Both types of larvae grow and survive well on Ctor, but only Psem-adapted larvae are able to survive on Psem. Larval foraging height: Ctor- and Psem-adapted larvae tend to feed at the top and base of their hosts, respectively. Female oviposition preference: Adult females prefer to lay eggs on the host to which they are adapted. Moreover, when forced to lay on Ctor, Ctor- and Psem-adapted females prefer individual plants at earlier and later phenological stages, respectively. Oviposition site height: Ctor-adapted females tend to lay their eggs at the top of their host near the point where they first land. Psem-adapted females invariably drop to explore the basal leaves of their host and lay near the ground. Clutch size: Ctor-adapted females lay 1–20 eggs per clutch while Psem-adapted females lay 30–100 eggs per clutch. This does not translate into a difference in either daily or lifetime fecundity since Ctor-adapted females lay more frequently than Psem-adapted females. No major phenotypic differences have been described in pupae or adult males.
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pbio-1000529-g002: Summary of traits addressed in this study.E. editha populations adapted to Collinsia torreyi (top row) and Pedicularis semibarbata (bottom row) have diverged in the six traits illustrated—two expressed in larvae and four expressed in adult females [40]. Larval performance: Both types of larvae grow and survive well on Ctor, but only Psem-adapted larvae are able to survive on Psem. Larval foraging height: Ctor- and Psem-adapted larvae tend to feed at the top and base of their hosts, respectively. Female oviposition preference: Adult females prefer to lay eggs on the host to which they are adapted. Moreover, when forced to lay on Ctor, Ctor- and Psem-adapted females prefer individual plants at earlier and later phenological stages, respectively. Oviposition site height: Ctor-adapted females tend to lay their eggs at the top of their host near the point where they first land. Psem-adapted females invariably drop to explore the basal leaves of their host and lay near the ground. Clutch size: Ctor-adapted females lay 1–20 eggs per clutch while Psem-adapted females lay 30–100 eggs per clutch. This does not translate into a difference in either daily or lifetime fecundity since Ctor-adapted females lay more frequently than Psem-adapted females. No major phenotypic differences have been described in pupae or adult males.

Mentions: The checkerspot butterfly Euphydryas editha provides a tractable system in which to begin addressing these gaps in understanding. The species is made up of multiple, allopatric populations in various stages of adaptation to distinct host plants [39]. Those populations adapted to Collinsia torreyi and Pedicularis semibarbata (Figure 1A) are distributed along the western slope of the Sierra Nevada in California (Figure 1B) in patches of coniferous woodland habitat where the two host plants are intermingled at the scale of inches to feet [40]. Despite host sympatry, the butterflies at any given site have evolved to lay eggs on just one of the two plant species and ignore the other, with the identity of the used host flip-flopping back and forth between sites (Figure 1B). The populations that use different hosts have diverged in several important host-related traits, ranging from larval performance and foraging height to adult female host preference, oviposition site height, and clutch size (Figure 2) [40]. Consistent host-associated differences in morphology and random genetic markers, on the other hand, remain elusive. A previous examination of >400 AFLPs revealed significant genetic differentiation among populations [39],[41], but this differentiation was not associated with the use of the two host plants examined here (subset of analyses from [41] summarized in Text S1).


Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

McBride CS, Singer MC - PLoS Biol. (2010)

Summary of traits addressed in this study.E. editha populations adapted to Collinsia torreyi (top row) and Pedicularis semibarbata (bottom row) have diverged in the six traits illustrated—two expressed in larvae and four expressed in adult females [40]. Larval performance: Both types of larvae grow and survive well on Ctor, but only Psem-adapted larvae are able to survive on Psem. Larval foraging height: Ctor- and Psem-adapted larvae tend to feed at the top and base of their hosts, respectively. Female oviposition preference: Adult females prefer to lay eggs on the host to which they are adapted. Moreover, when forced to lay on Ctor, Ctor- and Psem-adapted females prefer individual plants at earlier and later phenological stages, respectively. Oviposition site height: Ctor-adapted females tend to lay their eggs at the top of their host near the point where they first land. Psem-adapted females invariably drop to explore the basal leaves of their host and lay near the ground. Clutch size: Ctor-adapted females lay 1–20 eggs per clutch while Psem-adapted females lay 30–100 eggs per clutch. This does not translate into a difference in either daily or lifetime fecundity since Ctor-adapted females lay more frequently than Psem-adapted females. No major phenotypic differences have been described in pupae or adult males.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2964332&req=5

pbio-1000529-g002: Summary of traits addressed in this study.E. editha populations adapted to Collinsia torreyi (top row) and Pedicularis semibarbata (bottom row) have diverged in the six traits illustrated—two expressed in larvae and four expressed in adult females [40]. Larval performance: Both types of larvae grow and survive well on Ctor, but only Psem-adapted larvae are able to survive on Psem. Larval foraging height: Ctor- and Psem-adapted larvae tend to feed at the top and base of their hosts, respectively. Female oviposition preference: Adult females prefer to lay eggs on the host to which they are adapted. Moreover, when forced to lay on Ctor, Ctor- and Psem-adapted females prefer individual plants at earlier and later phenological stages, respectively. Oviposition site height: Ctor-adapted females tend to lay their eggs at the top of their host near the point where they first land. Psem-adapted females invariably drop to explore the basal leaves of their host and lay near the ground. Clutch size: Ctor-adapted females lay 1–20 eggs per clutch while Psem-adapted females lay 30–100 eggs per clutch. This does not translate into a difference in either daily or lifetime fecundity since Ctor-adapted females lay more frequently than Psem-adapted females. No major phenotypic differences have been described in pupae or adult males.
Mentions: The checkerspot butterfly Euphydryas editha provides a tractable system in which to begin addressing these gaps in understanding. The species is made up of multiple, allopatric populations in various stages of adaptation to distinct host plants [39]. Those populations adapted to Collinsia torreyi and Pedicularis semibarbata (Figure 1A) are distributed along the western slope of the Sierra Nevada in California (Figure 1B) in patches of coniferous woodland habitat where the two host plants are intermingled at the scale of inches to feet [40]. Despite host sympatry, the butterflies at any given site have evolved to lay eggs on just one of the two plant species and ignore the other, with the identity of the used host flip-flopping back and forth between sites (Figure 1B). The populations that use different hosts have diverged in several important host-related traits, ranging from larval performance and foraging height to adult female host preference, oviposition site height, and clutch size (Figure 2) [40]. Consistent host-associated differences in morphology and random genetic markers, on the other hand, remain elusive. A previous examination of >400 AFLPs revealed significant genetic differentiation among populations [39],[41], but this differentiation was not associated with the use of the two host plants examined here (subset of analyses from [41] summarized in Text S1).

Bottom Line: We then conducted field experiments to estimate the effects of intermediacy on fitness in nature.Our results revealed strong EPI under field conditions.Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females.

View Article: PubMed Central - PubMed

Affiliation: Center for Population Biology, University of California Davis, Davis, California, USA. lmcbride@rockefeller.edu

ABSTRACT
Gene flow between populations that are adapting to distinct environments may be restricted if hybrids inherit maladaptive, intermediate phenotypes. This phenomenon, called extrinsic postzygotic isolation (EPI), is thought to play a critical role in the early stages of speciation. However, despite its intuitive appeal, we know surprisingly little about the strength and prevalence of EPI in nature, and even less about the specific phenotypes that tend to cause problems for hybrids. In this study, we searched for EPI among allopatric populations of the butterfly Euphydryas editha that have specialized on alternative host plants. These populations recall a situation thought typical of the very early stages of speciation. They lack consistent host-associated genetic differentiation at random nuclear loci and show no signs of reproductive incompatibility in the laboratory. However, they do differ consistently in diverse host-related traits. For each of these traits, we first asked whether hybrids between populations that use different hosts (different-host hybrids) were intermediate to parental populations and to hybrids between populations that use the same host (same-host hybrids). We then conducted field experiments to estimate the effects of intermediacy on fitness in nature. Our results revealed strong EPI under field conditions. Different-host hybrids exhibited an array of intermediate traits that were significantly maladaptive, including four behaviors. Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females. We used our empirical data to construct a fitness surface on which different-host hybrids can be seen to fall in an adaptive valley between two peaks occupied by same-host hybrids. These findings demonstrate how ecological selection against hybrids can create a strong barrier to gene flow at the early stages of adaptive divergence.

Show MeSH