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PhD Research

RESEARCH

PhD (page last updated Oct. 2015)

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The Graduate Center, Queens College, CUNY, 2016

Advisor: David Lahti 

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Research question: How does a change in ecology affect the maintenance and evolution of male traits, female preferences, and their interaction?

 

A change in one or a few aspects of a species' ecology can lead to rapid trait evolution via natural selection, a phenomenon popularized by research on Darwin's finches (Grant & Grant 1993). Less is known, however, about how small (or large) changes in ecological features affect traits under sexual selection.

 

Competition for and availability of resources influence 

population density, which is positively related to the intensity of male competition and female choice, especially in promiscuous species. The small Indian mongoose (Herpestes auropunctatus, Fig. 1) is a promiscuous carnivore native to South Asia that has been introduced to dozens of (mostly) tropical island localities where it has become wildly invasive (Fig. 2). In contrast to its ancestral range where it faces intense interspecific competition and predation, in most of its introduced locations, this species is released from competition and predation leading to population densities that are between 30 and 120 times higher than in South Asia.

 

Little is known about the small Indian mongoose's behavior and nothing is known of its mating tendencies. For the first project of my doctoral research, I identified a behavior and trait associated with mate acquisition in males: scent marking and their scent marking tool, the anal pad (Owen & Lahti 2015, Fig. 3). Next, I compared mongooses from several populations in their resource-limited, low-density ancestral range of India to three resource-abundant, high-density islands of introduction (Hawaii, Jamaica, and St. Croix). Preliminary results reveal a shift in sexual selection on both behavioral and morphological characters in males from introduced locations: relative anal pad size has decreased and its level of condition-dependence has become significantly weaker, while relative testes size has increased (Fig. 4). These results suggest that the larger relative densities in areas of introduction have favored males to invest more in sperm volume (probably via increased sperm competition) and less in chemical advertisement.

 

In early 2016, I will travel to Mauritius for a final field season. Mongooses examined from my previous island field sites are thought to be descendants of the initial introduction from India to the Caribbean (Fig. 2), and thus my findings may be a product of a founder effect. Mauritian small Indian mongooses were introduced directly from India, and thus represent a separate lineage.

 

Since nothing is known about how mate choice occurs in this species, how this shift in sexual selection on males affects female mating decisions is unclear. Small Indian mongooses are not territorial but are known to be prolific scent markers. Thus, they likely use scent marking for inter- or intrasexual advertisement, or both. That is, males may mark to advertise their quality to other males to displace them, to females to be chosen as a mate, or both, and females might mark to displace other females, or to advertise their receptivity status to males, or both.

 

This summer in St. Croix, I conducted a behavioral study to attempt to understand the utility of their scent marking behavior. I placed anal gland secretion of an unfamiliar male or female mongoose inside traps in Sandy Point National Wildlife Refuge, to determine if there are any intersexual differences in investigative behaviors (e.g., being in close proximity to the scent, marking, sniffing, or touching it, etc.) to different sexes' scents, and I recorded the behaviors using trail cameras (Vid. 1). Analyses are underway, so stay tuned!

 

 

Additional project: Natural history of the small Indian mongoose in its native range.

 

The small Indian mongoose represents an interesting dichotomy regarding animal conservation: it is both protected and persecuted. In India, all species of mongoose are highly protected due to poaching; their fur is used to make high-quality paintbrushes. However, in the small Indian mongoose's dozens of introduced locations it has caused extirpations and even extinctions of many endemic species. As a result, the IUCN has named it one of the worst 100 invasive species on the planet.

 

Few data exist from their native range, and of these data, nearly all are anecdotal or observational. In India, I used trapping and radio telemetry to obtain the first data of their kind in their native range (Fig. 5). From these data, I hope to infer general natural history information, movement patterns and habitat preferences, and because I also tracked several individuals of the larger, sympatric grey mongoose (H. edwardsii), I hope to gain insights into how these species interact.

 

These data will be useful for both sides of the mongoose's conservation dichotomy: the information will update the current status of this animal where it is protected, and can help design more effective management techniques where it is invasive.

Fig. 1. Clockwise from top left: small Indian mongooses from Hilo, Hawaii; Dehradun, Uttarakhand, India; Frederiksted, St. Croix, USVI; and Kingston, Jamaica.

Fig. 2. Partial introduction history of the small Indian mongoose. Years indicate dates of introduction, parentheses indicate the approximate number of mongooses introduced. Mongooses can reproduce 2-3 times each year. From Thulin et al. (2006).

Fig. 3. Marked sexual size dimorphism in female (a) and male (b) anal pads of the small Indian mongoose. A: anus, AP: anal pad.

Fig. 4. International comparisons of small Indian mongoose males. Top: Analysis of covariance with anal pad area as the dependent variable and body condition and location as predictor variables. Bottom: Left: Residual anal pad area. Right: Residual testes size. Teses data were not collected in Hawaii. Letter differences correspond to significant differences (i.e., p < 0.001).

Vid. 1. Female small Indian mongoose investigating a trap baited with male anal gland secretion. She uses her anal pad to mark a twig near the trap. She also pauses to notice a car drive by in the distance.

Fig. 5. Top: Female small Indian mongoose fitted with VHF radio collar (tail is wet from rain). Bottom: GPS locations of both small Indian and grey mongooses in the village of Chandrabani, Uttarakhand, India. Colors represent different individuals.

Masters

Master's

 

Purdue University, 2010

Advisor: Rick Howard (retired)

 

Research question: How does a male trait arise in a population before it becomes the object of female choice?

 

Costly and conspicuous male secondary sexual characters are found throughout the animal kingdom. But why a specific character arose in a population over another, for example the posh decorative skills of bower birds, versus the long eye span of stalk-eyed flies, versus the array of dewlap colors in iguanids, is poorly understood. Investigating how females respond to novel characters can lend insights into this process.

 

Utilizing a relatively untapped technology in the field of sexual selection, genetic modification, I tested female preference in zebrafish (Danio rerio) for size-matched wildtype, brown and genetically modified, novel red males (Fig. 6) in four experiments (Owen et al. 2012). Experiments were designed to test different hypotheses regarding the origin of female choice. In all experiments, regardless of population history (isolation/drift), early social environment (sexual imprinting), or food color (associative learning unrelated to mating behaviors), females overwhelmingly preferred the novel, red males (Fig. 7).

 

Why might females have preferred males of novel coloration? The answer may lie not with novelty per se, but with the color red. In nature, zebrafish prey on zooplankton, among other organisms. Studies have shown that red coloration of zooplankton increases predation by zebrafish and other predatory fish. Perhaps the visual system of zebrafish evolved a bias to perceive red stimuli selectively as a result of a preference for red-colored prey. This prey-color-preference bias might then be transferred to red males, which has been suggested as an explanation for orange spots in guppies (Rodd et al. 2002). Another non-mutually exclusive explanation is that because several closely related species possess some degree of red coloration, preference for the color may be an ancestral relic. That is, females of an ancestral species initially evolved the preference for red color (perhaps as a bias towards red-colored prey), and as species diverged, red coloration subsequently evolved in males of some species, exploiting the females' sensory bias, the so-called sensory exploitation hypothesis (Fig. 8). Alternatively, the ancestral states may have included both red coloration and a preference for it, but the zebrafish lineage lost the coloration due to other selective pressures, perhaps predation, while females retained the preference.

Fig. 6. Wildtype (left) and genetically modifed, red (right) zebrafish. Photos courtesy of www.danios.info (left), and glofish.com (right).

Fig. 7. Time females spent associating with wildtype and red males. Each line represents an individual female in a trial. Exps. 1 and 2: females reared from separate populations differing in their proportion of the red morph (range 8-88%); exp. 3: females reared in specific ratios of all red, all wildtype, 75% red, or 75% wildtype; exp. 4: females fed green food rather than red. From Owen et al. (2012).

Fig. 8. The sensory exploitation hypothesis explained with 

Physalaemus frog species. Both the closely related P. petersi and P. pustulosus produce the bracketed "chuck" call suggesting that their common ancestor also possessed the trait. Female P. pustulosus prefer the chuck whereas female P. petersi do not. Neither P. coloradorum nor P. pustulatus produce the chuck, yet female P. coloradum prefer the chuck suggesting that females of the common ancestor of all species possessed a preference for the chuck. T-: chuck absent, T+: chuck present, P-: preference absent, P+ preference present. From Kirkpatrick and Ryan (1991)

Undergraduate

Undergraduate

 

Northern Illinois University, 2008

Advisor: Bethia King

 

Research question: What changes in locomotion contribute to sexual inhibition?

 

Sexual inhibition is the situation in which an individual chooses not to mate despite the opportunity to do so. In the parasitoid wasp Spalangia endius (Fig. 9), males undergo a period of sexual inhibition immediately after mating. This behavior is suggested to avoid remating with the same female as females typically mate only once. However, the changes to male movements during this period are not known. I collected data from an experiment designed to understand what locomotor differences exist between virgin males and mated males undergoing sexual inhibition (King & Owen 2012). One virgin and one mated male were placed into a petri dish, either with a female present or absent, and three aspects of locomotion were recorded for each male: restlessness (time spent locomoting), speed, and path directness.

 

We found that in the presence of a female, relative to virgin males, mated males tended to be less restless (i.e., locomoted less) and less direct in their paths but were faster moving. Differences between virgin and mated males, however, were only detected in the presence of a female suggesting that post-mating locomoter changes are not intrinsic changes to males but rather changes in how males respond to cues from females. After this study was conducted, an arresting female sex pheromone was identified in this species, and while we do not know if virgin and mated males respond differently to this pheromone, it is a plausible explanation.

Fig. 9. A Spalangia endius parasitoid wasp sits atop the pupa of its host, the common house fly (Musca domestica). Photo from bugsforbugs.com.au.

Fig. 10. Comparisons of mated (y-axis) and virgin (x-axis) males in restlessness (top), speed (left), and path directness (right). Each point represents males in a single trial. Diagonal line represents a reference of no difference. From King & Owen (2012).

References

References

 

B.R. Grant and P.R. Grant. 1993. Evolution of Darwin's finches caused by a rare climatic event. Proceedings of the Royal Society London B. 251: 111-117.

 

King, B.H. and M.A. Owen. 2012. Post-mating changes in restlessness, speed and route directness in males of the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae). Journal of Insect Behavior. 25: 309-319. PDF

 

Kirkpatrick, M. and M.J. Ryan. 1991. The evolution of mating preferences and the paradox of the lek. Nature. 350: 33-38.

 

Owen, M.A. and D.C. Lahti. 2015. Sexual dimorphism and condition dependence in the anal pad of the small Indian mongoose (Herpestes auropunctatus). Canadian Journal of Zoology. 93(5): 397-402. PDF

 

Owen, M.A., K. Rohrer, and R.D. Howard. 2012. Mate choice for a novel male phenotype in zebrafish, Danio rerioAnimal Behaviour. 83(3): 811-820. PDF

 

Rodd, F.H., K.A. Hughes, G.F. Grether, and C.T. Baril. 2002. A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proceedings of the Royal Society London B. 269: 475-481.

 

Thulin, C., D. Simberloff, A. Barun, G. McCracken, M. Pascal, and M.A. Islam. 2006. Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species. Molecular Ecology. 15(13): 3947-3956.

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