Evolving while invading: rapid adaptive evolution in juvenile development time for a biological control organism colonizing a high‐elevation environment

Abstract

We report evidence of adaptive evolution in juvenile development time on a decadal timescale for the cinnabar moth Tyria jacobaeae (Lepidoptera: Arctiidae) colonizing new habitats and hosts from the Willamette Valley to the Coast Range and Cascades Mountains in Oregon. Four lines of evidence reveal shorter egg to pupa juvenile development times evolved in the mountains, where cooler temperatures shorten the growing season: (i) field observations showed that the mountain populations have shorter phenological development; (ii) a common garden experiment revealed genetic determination of phenotypic differences in juvenile development time between Willamette Valley and mountain populations correlated with the growing season; (iii) a laboratory experiment rearing offspring from parental crosses within and between Willamette Valley and Cascades populations demonstrated polygenic inheritance, high heritability, and genetic determination of phenotypic differences in development times; and (iv) statistical tests that exclude random processes (founder effect, genetic drift) in favor of natural selection as explanations for observed differences in phenology. These results support the hypothesis that rapid adaptation to the cooler mountain climate occurred in populations established from populations in the warmer valley climate. Our findings should motivate regulators to require evaluation of evolutionary potential of candidate biological control organisms prior to release.

Thermal plasticity and microevolution enhance establishment success and persistence of a water hyacinth biological control agent

“…Even shorter time-frames for acclimation have been shown in other studies, with Weldon et al (2011) observing thermal acclimation in the tephritid flies Ceratitis capitata Wiedemann and Ceratitis rosa Karsch after only a single day. Development rate of Tyria jacobaeae (L.), a control agent for ragwort, Jacobaea vulgaris Gaertn., in the USA, differed depending on the climate at the site in which they had established after release (McEvoy et al, 2012). Similar physiological damage has been and Enseleni (E)] of Eccritotarsus catarinensis for summer and winter using the reduced major axis regression method (Ikemoto & Takai, 2000).…”

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

“…For example, studies simply documenting reduced genetic diversity (Roehrdanz et al, 2006;Franks et al, 2011;Ma et al, 2013), the retention of genetic diversity (Taylor et al, 2011), or the presence of geographic structure post-introduction (Vorsino et al, 2014) do not by themselves provide evidence of adaptive evolution. Thus, there is little strong evidence for post-introduction adaptation in biocontrol agents in field populations (but see Bean et al, 2012;McEvoy et al, 2012;Sz} ucs et al, 2012a). Thus, there is little strong evidence for post-introduction adaptation in biocontrol agents in field populations (but see Bean et al, 2012;McEvoy et al, 2012;Sz} ucs et al, 2012a).…”

“…Here, we provide examples indicative of adaptations to these novel abiotic conditions. ), were released at both low and high elevations, and rapidly evolved differences in life-history traits in response to the cooler climate and shorter growing seasons at high elevations (McEvoy et al, 2012;Sz} ucs et al, 2012a). Furthermore, they were able to trace the genetic history of several invasive populations to more accurately identify niche shifts and phenotypic shifts between native and invasive populations to demonstrate local adaptation.…”

Theoretical contributions to biological control success

“…Studying invasive species in both native and introduced ranges is a longstanding practice in biological control and recently recommended by ecologists for studying the mechanisms that regulate ecological and evolutionary dynamics of invasive plants (Hierro et al 2005;Williams et al 2010). Recently, the tansy ragwort system has been used to study the role of rapid evolution in ecological dynamics (McEvoy et al 2012b;Rapo et al 2010;Szucs et al 2012).…”