Environmental heterogeneity influences coevolution and local adaptation in host–parasite systems. This also concerns applied issues, because the geographic range of parasites may depend on their capacity to adapt to abiotic conditions. We studied temperature‐specific adaptation in the wheat yellow/stripe rust pathogen, Puccinia striiformis f.sp. tritici (PST). Using laboratory experiments, PST isolates from northern and southern France were studied for their ability to germinate and to infect bread and durum wheat cultivars over a temperature gradient. Pathogen origin × temperature interactions for infectivity and germination rate suggest local adaptation to high‐ versus low‐temperature regimes in south and north. Competition experiments in southern and northern field sites showed a general competitive advantage of southern over northern isolates. This advantage was particularly pronounced in the southern ‘home’ site, consistent with a model integrating laboratory infectivity and field temperature variation. The stable PST population structure in France likely reflects adaptation to ecological and genetic factors: persistence of southern PST may be due to adaptation to the warmer Mediterranean climate; and persistence of northern PST can be explained by adaptation to commonly used cultivars, for which southern isolates are lacking the relevant virulence genes. Thus, understanding the role of temperature‐specific adaptations may help to improve forecast models or breeding programmes.

Investigating the origin and dispersal pathways is instrumental to mitigate threats and economic and environmental consequences of invasive crop pathogens. In the case of Puccinia striiformis causing yellow rust on wheat, a number of economically important invasions have been reported, e.g., the spreading of two aggressive and high temperature adapted strains to three continents since 2000. The combination of sequence‐characterized amplified region (SCAR) markers, which were developed from two specific AFLP fragments, differentiated the two invasive strains, PstS1 and PstS2 from all other P. striiformis strains investigated at a worldwide level. The application of the SCAR markers on 566 isolates showed that PstS1 was present in East Africa in the early 1980s and then detected in the Americas in 2000 and in Australia in 2002. PstS2 which evolved from PstS1 became widespread in the Middle East and Central Asia. In 2000, PstS2 was detected in Europe, where it never became prevalent. Additional SSR genotyping and virulence phenotyping revealed 10 and six variants, respectively, within PstS1 and PstS2, demonstrating the evolutionary potential of the pathogen. Overall, the results suggested East Africa as the most plausible origin of the two invasive strains. The SCAR markers developed in the present study provide a rapid, inexpensive, and efficient tool to track the distribution of P. striiformis invasive strains, PstS1 and PstS2.

Costs of adaptation play an important role in host-parasite coevolution. For parasites, evolving the ability to circumvent host resistance may trade off with subsequent growth or transmission. Such costs of virulence (sensu plant pathology) limit the spread of all-infectious genotypes and thus facilitate the maintenance of genetic polymorphism in both host and parasite. We investigated costs of three virulence factors in Puccinia striiformis f.sp.tritici, a fungal pathogen of wheat (Triticum aestivum).

Yellow rust is a devastating wheat disease. Since 2000, Puccinia striiformis f. sp. tritici strains PstS1 and PstS2 have become adapted to high temperatures and have spread worldwide. By 2011, Warrior strains had invaded both warm and cold areas of Europe. This study questioned whether thermal aptitude promoted the spread of Warrior strains, similar to PstS1/PstS2, by comparing infection efficiency ( IE ) at five temperatures and latent period ( LP ) under warm and cold regimes for Warrior isolates and pre‐2011 reference strains on two susceptible wheat varieties. The Warrior isolates showed a range of IE and LP responses to temperature that was intermediate between the northern reference isolates adapted to cold conditions and both the southern and invasive PstS2 isolates adapted to warm conditions. Warrior isolates had the highest IE under optimal temperatures of 10 and 15 °C, and displayed reduced infectivity under the warmest (20 °C) and coldest (5 °C) temperatures. Warrior strains acted as thermal generalists and the reference isolates acted as specialists. An IE thermal response was used to simulate the development of each isolate under future climate scenarios in a temperate and Mediterranean region. Isolates had the same ranking for yearly IE over the three 30‐year periods (1971–2000, 2021–2050, 2071–2100) and both locations, with a slight infection increase in the future. However, in the future IE s increased in earlier months. The thermal generalist profile of Warrior isolates for IE was confirmed, with an intermediate capacity to tolerate warming climate, whereas the southern isolates are better adapted to warm conditions, but do not have the virulences necessary to develop on current varieties.