The Evolution and Maintenance of Delayed Implantation in the Mustelidae (Mammalia: Carnivora)

Abstract

Diapause, the temporary cessation of development at an early life-history stage, is widespread among animals and plants. The range of taxa exhibiting various forms of diapause indicates its enormous ecological significance and highlights its value as a model for examining life-history trait evolution. However, despite the impact of diapause on species ecology, there is little understanding of its adaptive value in many groups. Furthermore, the relative roles of phylogeny and ecology in determining the contemporary expression of the trait remain unresolved. Delayed implantation (DI) is a type of diapause found in several orders of mammals. It is particularly prevalent in the Mustelidae, with mustelids making up more than half of all mammals known to exhibit DI. This taxon is thus ideal for examining life-history predictors of DI and investigating the mode of evolution. Both maximum likelihood and maximum parsimony methods of ancestral state reconstruction indicated DI to be plesiomorphic in the mustelids, although multiple state changes are required to explain its contemporary distribution. After controlling for phylogeny, species with and without DI could be discriminated using just three variables: longevity, maximum latitude of the geographical distribution, and a term describing maternal investment. Our analyses supported the hypothesis that DI is more prevalent in seasonal climates. We also showed that longer-lived species are more likely to exhibit DI, suggesting a time cost to the trait. We found no correlate for the highly variable duration of DI, which remains unexplained. Although ecological factors can predict the distribution of DI in modern mustelids, phylogenetic constraint is likely to play an important role.

Embryonic Diapause Is Conserved across Mammals

“…Indeed, the optimal timing for reproduction may vary from year to year and from place to place. The flexible occurrence of ED in the same species supports the idea that ecological factors have a significant role in the determination of this trait [13], [14], [19]. This should be taken into account when classifying a species as diapausing or non-diapausing.…”

Latitudinal variation in photoperiodic response of the three‐spined sticklebackGasterosteus aculeatusin western North America

“…In lizards, with increasing latitude, day length has an increasing effect on metabolic rate in Sceloporus undulatus (Angilleta, 2001), on growth rate in Lacerta viviparia (Uller & Olsson, 2003) and on ability to maintain a constant body temperature during the spring in Sceloporus occidentalis occidentalis (Lashbrook & Livezey, 1970). In mammals, with increasing latitude, short days have an increasing tendency to induce gonadal regression in mice Peromyscus leucopus and Peromyscus maniculatus (Lynch et al , 1981; Sullivan & Lynch, 1986; Heideman et al , 1999; Lowrey et al , 2000) or embryonic dormancy in multiple species of mustelids (Thom et al , 2004). Hence, the general vertebrate pattern, including that of G. aculeatus , is a pattern of an increasing influence of day length in the timing of important seasonal life‐history events with increasing latitude among intraspecific populations.…”

Does seasonality explain the evolution and maintenance of delayed implantation in the family Mustelidae (Mammalia: Carnivora)?

“…However, birth season is influenced not only by true environmental seasonality, but also by other environmental gradients such as latitude and precipitation. Thom et al (2004) used latitude as a surrogate for seasonality and concluded that their “… analyses supported the hypothesis that delayed implantation is more prevalent in seasonal climates” (Thom et al 2004: 175). Seasonality, defined as the variation in environmental conditions within a year's time, is a variable independent of biological events.…”

“…Additionally, we provide structural equation model evidence supporting the role of environmental variables in the evolution or maintenance of delayed implantation for species living with greater seasonality, or its loss in species occupying less seasonal environments. Life history traits of Mustelidae suggest that, once we control for phylogenetic effects, the environmental pressures associated with life in northern environments, be they seasonality, primary productivity, snowfall or latitudes (Thom et al 2004), emerge as the unifying theme in environmental traits characterizing mustelids with delayed implantation.…”

“…In mammalian species with relatively fixed gestation length, time of mating determines time of parturition. In contrast, species with delayed implantation may uncouple mating and parturition (Aitken 1974, Sandell 1990, Ferguson et al 1996, Thom et al 2004) and thus be able to shift their mating season away from the snow season to a time when males are more mobile and can better find receptive females. Evolutionary pressures related to seasonality have been directly linked to mammalian reproduction and the presence of reproductive traits (Beck et al 2003, Larivière and Ferguson 2003, McNamara et al 2004, Ferguson and Larivière 2004a).…”