Effects of reproductive interference on the competitive displacement between two invasive whiteflies

Abstract

Reproductive interference is one of the major factors mediating species exclusion among insects. The cryptic species Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) of the whitefly Bemisia tabaci complex have invaded many parts of the world and often exhibit niche overlap and reproductive interference. However, contrasting patterns of competitive displacement between the two invaders have been observed between regions such as those in USA and China. Understanding the roles of reproductive interference in competitive interactions between populations of the two species in different regions will help unravel other factors related to their invasion. We integrated laboratory population experiments, behavioural observations and simulation modelling to investigate the role of reproductive interference on species exclusion between MEAM1 and MED in China. In mixed cohorts of the two species MEAM1 always excluded MED in a few generations when the initial proportion of MEAM1 was ⩾0.25. Even when the initial proportion of MEAM1 was only 0.10, however, MEAM1 still had a higher probability of excluding MED than that for MED to exclude MEAM1. Importantly, we show that as MEAM1 increased in relative abundance, MED populations became increasingly male-biased. Detailed behavioural observations confirmed that MEAM1 showed a stronger reproductive interference than MED, leading to reduced frequency of copulation and female progeny production in MED. Using simulation modelling, we linked our behavioural observations with exclusion experiments to show that interspecific asymmetric reproductive interference predicts the rate of species exclusion of MED by MEAM1. These findings not only reveal the importance of reproductive interference in the competitive interactions between the two invasive whiteflies as well as the detailed behavioural mechanisms, but also provide a valuable framework against which the effects of other factors mediating species exclusion can be explored.

Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005–2014

“…In the past two decades, the B biotype spread into at least 54 countries, followed by the invasion of the Q biotype, which has been found in at least 10 countries1. These two biotypes differ in a range of biological characteristics, including host plant range and adaptability, ability to transmit plant virus, copulation efficiency, composition of harbored symbionts, and expression of resistance to heat shock and insecticide34567891011121314. These differences contribute to the competitive outcomes between the two biotypes in various habitats.…”

Natal Host Plants Can Alter Herbivore Competition

“…Although this possibility seems improbable, it is worth noting that the most rapid increase in MED frequency occurred within the first two generations of the experiment (fig 1B). This would be consistent with transgenerational effects that primarily affect the first and second generations; although these effects may dissipate afterwards, MED may by then possess such a large numerical advantage that it is able to displace the ‘competitively dominant’ MEAM1 [31]. …”

“…This provided MEAM1 a numerical advantage that helped it excluded MED over the course of several generations. Second, several studies have documented asymmetric reproductive interference between MEAM1 and MED [31, 35]. Although MEAM1-MED crosses produce virtually no viable offspring [36], MEAM1 males are more aggressive than MED males in courting females of both species; as a result, MEAM1 males interfere more with intra-specific mating attempts by MED than vice versa [35].…”

“…Because B . tabaci is haplodiploid, fertilized eggs become female and unfertilized eggs become male; the inability of MED females to compensate for reproductive interference by MEAM1 males yields a male-skewed sex ratio that decreases MED population growth [31, 35]. Laboratory-parameterized simulations of MEAM1-MED competition reveal that while MEAM1’s growth and reproductive advantages are both important, the asymmetric impact of MEAM1’s reproductive interference on MED can itself produce competitive exclusion.…”

“…If poinsettia does select for individuals with that rapidly feed on and process phloem, this adaptation may prove beneficial on a range of host plants. Given the role played by asymmetric reproductive interference in the MEAM1-MED interaction on cotton [31, 35], it is also possible that poinsettia-derived MED differ in some aspect of their mating behavior. Long-term rearing on poinsettia might select for MED males that are particularly aggressive in their courting behavior, for instance, or might favor MED females with a stronger preference for males of their own species.…”