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

Abstract

Understanding the evolutionary pressures that may have led to the development and retention of delayed implantation in mammals remains an enigmatic puzzle for evolutionary ecologists. Recent studies suggest a strong role of environmental conditions but other attributes of species, notably body size and life history traits, may obscure primary mechanisms. Following the recommendation of Lindenfors et al., we examined environmental correlates related to the evolution of delayed implantation and its subsequent maintenance or loss in the family Mustelidae (Mammalia: Carnivora). We focused on the Mustelidae because evolution and subsequent loss of delayed implantation occurred most commonly within this group. Data on 34 species of mustelids from around the world suggest that delayed implantation may have evolved when optimal times for mating and birthing are separated by more than a gestation period, characteristic of environments with long winters that reduce the opportunities to find mates. Environmental characteristics (seasonality, temperature, snow, latitude, and primary productivity) were highly intercorrelated but seasonality was the best predictor of the evolution or loss of delayed implantation via population traits. Here, structural equations on phylogenetic independent contrasts revealed that high seasonality was correlated with low population density and large individual home range size, which in turn was correlated with presence/absence of delayed implantation. We argue that the evolution of delayed implantation provides the reproductive means to mate during the season (summer) with the greatest prospects for females to ‘choose’ mates when living in high‐latitude seasonal environments that generally reduce these opportunities (i.e. low population density and large ranges). Body mass of female mustelids did not differ between species with and without delayed implantation, refuting the hypothesis that loss of delayed implantation is an evolutionary by‐product of evolving to smaller size. We conclude that understanding the environmental selection pressures responsible for the evolution of life history traits related to density and spacing behaviour allows for a more complete picture of the evolution and subsequent loss of delayed implantation.

How Social Behaviour Links Environment and Body Size in Mammalian Carnivores

“…A possibly mechanism for terrestrial mammals is seasonal snow conditions that affect the movements of animals and subsequently lead to adaptations, such as delayed implantation, to overcome limitations posed by social behaviour [14]. Similarly, Bergmann's rule may be more related to seasonality than to temperature [15,16].…”

“…For mating, the one sex (usually males) that is responsible for finding the other sex (usually females) needs to move about more during the mating season [14,20]. Therefore, a consequence of living at low densities and occupying large ranges is that greater sexual size dimorphism will also occur with increasing latitude.…”

Morphological variability of baculum (os penis) in the polecat Mustela putorius

“…One of the species in which baculum size and shape have been described (SUMIÑSKI 1968;WAL-TON 1968;KIERDORF 1996;BARYSHNIKOV et al 2003;FERGUSON et al 2006) is the polecat (Mustela putorius LINNAEUS, 1758). This species can be found throughout most of Europe.…”

“…Comparisons of the species with other carnivores based on good sample sizes have been published together with descriptions of the main morphological parameters, including information on the baculum. Studies have examined the influence of age on baculum size (SUMIÑSKI 1968;WALTON 1968;WOLSAN 1993), regeneration pattern, or described general characteristics of the os penis, such as length (KIERDORF 1996), and evolutionary relationships with other mustelids (BARYSHNIKOV et al 2003;FERGUSON et al 2006).…”

The evolution of embryo implantation

“…At least in some species, delayed implantation is most likely correlated with the degree of seasonality of the environment. This is especially well documented in the Carnivora, where mustelids (weasels and relatives) and mephitids (skunks) living in temperate environments tend to retain delayed implantation (Ferguson et al ., 2006, Thom et al ., 2004), some delaying implantation for up to 11 months (McGowen et al ., 2013, Sandell, 1990). In other species with multiple litters per year, such as marsupials, rodents, and insectivores, delayed implantation occurs before the previous litter is weaned, and is likely an energy saving mechanism (Sandell, 1990).…”