Complex inheritance of larval adaptation in Plutella xylostella to a novel host plant

Abstract

Studying the genetics of host shifts and range expansions in phytophagous insects contributes to our understanding of the evolution of host plant adaptation. We investigated the recent host range expansion to pea, in the pea-adapted strain (P-strain) of the crucifer-specialist diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Larval survivorship on the novel host plant pea and a typical crucifer host (kale) was measured in reciprocal F(1), F(2) and backcrosses between the P-strain and a strain reared only on crucifers (C-strain). Reciprocal F(1) hybrids differed: offspring from P-strain mothers survived better on pea, indicating a maternal effect. However, no evidence for sex-linkage was found. Backcrosses to the P-strain produced higher survivorship on pea than C-strain backcrosses, suggesting recessive inheritance. In a linkage analysis with amplified fragment length polymorphism markers using P-strain backcrosses, two, four and five linkage groups contributing to survival on pea were identified in three different families respectively, indicating oligogenic inheritance. Thus, the newly evolved ability to survive on pea has a complex genetic basis, and the P-strain is still genetically heterogeneous and not yet fixed for all the alleles enabling it to survive on pea. Survivorship on kale was variable, but not related to survivorship on pea. This pattern may characterize the genetic inheritance of early host plant adaptation in oligophagous insect species.

Figure 1

Mating design for cross C1 (a) and cross C2 (b). Males and females of the pea-adapted host strain (P) and cabbage-adapted strain (C) were crossed in every possible direction. In C1, F₁ and backcross progenies were distributed equally on pea (½) and kale (½) plants. In cross C2, all F₁ and P-strain individuals used in the backcross were reared on kale. F₂ and backcross progenies were distributed in a 2:1 ratio (⅔ on pea and ⅓ on kale).

Figure 2

Survival rates of larvae per family in (a) F₁ generation of cross C1; (b) backcross generation of cross C1; and (c) backcross generation of cross C2. Diamonds: survival rates on kale plants; squares: survival rate on pea plants. Each vertical pair of a square and a diamond, connected with a dotted line, represents the survival rate of larvae from one family on pea and kale, respectively.

Figure 3

Association between chromosomes of the three analyzed backcross families BC_01, BC_02 and BC_03 in cross C2 and the trait ‘survival on pea'. The P-values were calculated using Fisher's exact test. Significant P-values indicate over-representation of chromosomes inherited from the P-strain grandparent via the F₁ female in pea survivors relative to kale survivors. P-values corresponding to chromosomes based on pooling homologous linkage groups over families are shown below, with the families that were combined indicated with an X. The Bonferroni-corrected probability value for six independent tests is shown as P=0.0083.

Figure 4

Bulked segregant analysis of AFLPs to identify homologous linkage groups. Each LG in each family is represented by two bulks: one with individuals that carry the AFLP band and the other where the band is absent. Linkage groups within families are listed across the top of the figure. AFLP markers with concordant patterns in two of the bulks are listed down the side, grouped according to chromosome. Primer combinations and band sizes (in bp) are given along with a slice of the gel image showing the AFLP pattern. Circles placed immediately below the relevant band denote where a specific presence/absence pattern (filled circle vs open circle) occurs, indicating the correspondence between the same linkage group in two different families. Only LG5 in BC_01 fails to match with any of the other patterns shown.