Nature beats nurture: a case study of the physiological fitness of free-living and laboratory-reared maleAnopheles gambiae s.l.

Abstract

SUMMARY Laboratory experimentation forms the basis for most of our knowledge of the biology of many organisms, in particular insects. However, the accuracy with which laboratory-derived estimates of insect life history and behaviour can predict their fitness and population dynamics in the wild is rarely validated. Such comparison is especially important in cases where laboratory-derived information is used to formulate and implement strategies for the genetic control of insects in nature. We have conducted a comparative study of the reproductive potential and life history of male Anopheles gambiaeGilies sensu lato mosquitoes from both standardized laboratory conditions and from natural field settings. We measured three indirect indicators of male mosquito fitness: energetic reserves, body size and survival, in a bid to determine whether the demographics and energetic limitations of wild males can be correctly predicted from their laboratory counterparts. Crucially, the body size and lipid reserves of wild males were substantially greater than those reared under standard laboratory conditions. We caution that the energetic limitations of insects as identified in the laboratory may underestimate their resilience in the wild, and discuss the implications of this phenomenon with respect to vector-borne disease control programmes based on genetic control of mosquitoes.

Desiccation tolerance as a function of age, sex, humidity and temperature in adults of the African malaria vectorsAnopheles arabiensisPatton andAnopheles funestusGiles

“…Some physiological traits are known to be more affected by laboratory conditions than others (Hoffmann et al, 2001;Huho et al, 2007; but see Terblanche et al, 2006;Parkash and Ranga, 2014). Our data suggest that the maintenance of A. arabiensis under colony conditions over several decades has had an effect on body size, which in turn affects survival time, but that other traits such as water loss tolerated are not affected.…”

“…Other work has also found differences among laboratory and wild strains of A. gambiae in size and in internal nutrient resources (Huho et al, 2007). The size differences in A. gambiae males are similar to those found here for A. arabiensis males (larger individuals in the wild strain), but A. arabiensis females varied in the opposite direction [Huho et al did not investigate females (Huho et al, 2007)]. Such trait variation among laboratory and field strains, although often small in effect, may nonetheless be important and should therefore be the subject of further investigation to improve the translation of laboratory to field…”

“…One major concern with the current study might be that the findings reflect the situation only with the laboratory strains, given that laboratory adaptation has been recorded in several, though not all, species for several traits [see elsewhere for discussion Parkash and Ranga, 2014) and for differing extents of laboratory adaptation in Anopheles species (Huho et al, 2007;Lyons et al, 2012)]. We investigated the extent of variation among laboratory and wild strains of A. arabiensis for the traits examined here.…”

“…Nonetheless, it is important to note the size differences among the laboratory and wild strains, and that for thermal tolerance traits of this species, laboratory strains showed significant differences from wild strains, but these differences were not large enough in effect size to render thermal tolerance work in the laboratory irrelevant to the field situation (Lyons et al, 2012). Other work has also found differences among laboratory and wild strains of A. gambiae in size and in internal nutrient resources (Huho et al, 2007). The size differences in A. gambiae males are similar to those found here for A. arabiensis males (larger individuals in the wild strain), but A. arabiensis females varied in the opposite direction [Huho et al did not investigate females (Huho et al, 2007)].…”

Non-destructive Determination of Age and Species of Anopheles gambiae s.l. Using Near-infrared Spectroscopy

“…gambiae s.s. male testes and the relative size of their sperm reservoirs. 61 These models can classify males into young (≤ 4 days of age) and old (> 4 days of age) groups. It is doubtful that the spermatocysts and sperm reservoir are contributing to our NIR classifications because of their small size relative to the insect cuticle (NIR spectra are affected by the amount of material absorbing NIR radiation).…”